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  • 1.
    Alavioon, Ghazal
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Garcia, Andrea Cabrera
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    LeChatelier, Magali
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Maklakov, Alex A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. Univ East Anglia, Sch Biol Sci, Norwich Res Pk, Norwich, Norfolk, England.
    Immler, Simone
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. Univ East Anglia, Sch Biol Sci, Norwich Res Pk, Norwich, Norfolk, England.
    Selection for longer lived sperm within ejaculate reduces reproductive ageing in offspring2019In: EVOLUTION LETTERS, ISSN 2056-3744, Vol. 3, no 2, p. 198-206Article in journal (Refereed)
    Abstract [en]

    Males produce numerous sperm in a single ejaculate that greatly outnumber their potential egg targets. Recent studies found that phenotypic and genotypic variation among sperm in a single ejaculate of a male affects the fitness and performance of the resulting offspring. Specifically, within-ejaculate sperm selection for sperm longevity increased the performance of the resulting offspring in several key life-history traits in early life. Because increased early-life reproductive performance often correlates with rapid ageing, it is possible that within-ejaculate sperm selection increases early-life fitness at the cost of accelerated senescence. Alternatively, within-ejaculate sperm selection could improve offspring quality throughout the life cycle, including reduced age-specific deterioration. We tested the two alternative hypotheses in an experimental setup using zebrafish Danio rerio. We found that within-ejaculate sperm selection for sperm longevity reduced age-specific deterioration of fecundity and offspring survival but had no effect on fertilization success in males. Remarkably, we found an opposing effect of within-ejaculate sperm selection on female fecundity, where selection for sperm longevity resulted in increased early-life performance followed by a slow decline, while females sired by unselected sperm started low but increased their fecundity with age. Intriguingly, within-ejaculate sperm selection also reduced the age-specific decline in fertilization success in females, suggesting that selection for sperm longevity improves at least some aspects of female reproductive ageing. These results demonstrate that within-ejaculate variation in sperm phenotype contributes to individual variation in animal life histories in the two sexes and may have important implications for assisted fertilization programs in livestock and humans.

  • 2.
    Alavioon, Ghazal
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Hotzy, Cosima
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Nakhro, Khriezhanuo
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Rudolf, Sandra
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Scofield, Douglas
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Zajitschek, Susanne
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. Spanish Natl Res Council, Donana Biol Stn, Seville 41092, Spain.
    Maklakov, Alex A
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. Univ East Anglia, Sch Biol Sci, Norwich NR4 7TJ, Norfolk, England.
    Immler, Simone
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. Univ East Anglia, Sch Biol Sci, Norwich NR4 7TJ, Norfolk, England.
    Haploid selection within a single ejaculate increases offspring fitness2017In: Proceedings of the National Academy of Sciences of the United States of America, ISSN 0027-8424, E-ISSN 1091-6490, no 30, p. 8053-8058Article in journal (Refereed)
    Abstract [en]

    An inescapable consequence of sex in eukaryotes is the evolution of a biphasic life cycle with alternating diploid and haploid phases. The occurrence of selection during the haploid phase can have far-reaching consequences for fundamental evolutionary processes including the rate of adaptation, the extent of inbreeding depression, and the load of deleterious mutations, as well as for applied research into fertilization technology. Although haploid selection is well established in plants, current dogma assumes that in animals, intact fertile sperm within a single ejaculate are equivalent at siring viable offspring. Using the zebrafish Danio rerio, we show that selection on phenotypic variation among intact fertile sperm within an ejaculate affects offspring fitness. Longer-lived sperm sired embryos with increased survival and a reduced number of apoptotic cells, and adult male offspring exhibited higher fitness. The effect on embryo viability was carried over into the second generation without further selection and was equally strong in both sexes. Sperm pools selected by motile phenotypes differed genetically at numerous sites throughout the genome. Our findings clearly link within-ejaculate variation in sperm phenotype to offspring fitness and sperm genotype in a vertebrate and have major implications for adaptive evolution.

  • 3.
    Berg, Elena C.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Maklakov, Alexei A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Sexes suffer from suboptimal lifespan because of genetic conflict in a seed beetle2012In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 279, no 1745, p. 4296-4302Article in journal (Refereed)
    Abstract [en]

    Males and females have different routes to successful reproduction, resulting in sex differences in lifespan and age-specific allocation of reproductive effort. The trade-off between current and future reproduction is often resolved differently by males and females, and both sexes can be constrained in their ability to reach their sex-specific optima owing to intralocus sexual conflict. Such genetic antagonism may have profound implications for evolution, but its role in ageing and lifespan remains unresolved. We provide direct experimental evidence that males live longer and females live shorter than necessary to maximize their relative fitness in Callosobruchus maculatus seed beetles. Using artificial selection in a genetically heterogeneous population, we created replicate long-life lines where males lived on average 27 per cent longer than in short-life lines. As predicted by theory, subsequent assays revealed that upward selection on male lifespan decreased relative male fitness but increased relative female fitness compared with downward selection. Thus, we demonstrate that lifespan-extending genes can help one sex while harming the other. Our results show that sexual antagonism constrains adaptive life-history evolution, support a novel way of maintaining genetic variation for lifespan and argue for better integration of sex effects into applied research programmes aimed at lifespan extension.

  • 4.
    Berger, David
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Berg, Elena C
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Widegren, William
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Arnqvist, Göran
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Maklakov, Alexei A
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Multivariate intralocus sexual conflict in seed beetles2014In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 68, no 12, p. 3457-69Article in journal (Refereed)
    Abstract [en]

    Intralocus sexual conflict (IaSC) is pervasive because males and females experience differences in selection but share much of the same genome. Traits with integrated genetic architecture should be reservoirs of sexually antagonistic genetic variation for fitness, but explorations of multivariate IaSC are scarce. Previously, we showed that upward artificial selection on male life span decreased male fitness but increased female fitness compared with downward selection in the seed beetle Callosobruchus maculatus. Here, we use these selection lines to investigate sex-specific evolution of four functionally integrated traits (metabolic rate, locomotor activity, body mass, and life span) that collectively define a sexually dimorphic life-history syndrome in many species. Male-limited selection for short life span led to correlated evolution in females toward a more male-like multivariate phenotype. Conversely, males selected for long life span became more female-like, implying that IaSC results from genetic integration of this suite of traits. However, while life span, metabolism, and body mass showed correlated evolution in the sexes, activity did not evolve in males but, surprisingly, did so in females. This led to sexual monomorphism in locomotor activity in short-life lines associated with detrimental effects in females. Our results thus support the general tenet that widespread pleiotropy generates IaSC despite sex-specific genetic architecture.

  • 5.
    Berger, David
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Grieshop, Karl
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Lind, Martin I.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Goenaga, Julieta
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics.
    Maklakov, Alexei A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Arnqvist, Göran
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Intralocus Sexual Conflict and Environmental Stress2014In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 68, no 8, p. 2184-2196Article in journal (Refereed)
    Abstract [en]

    Intralocus sexual conflict (IaSC) occurs when selection at a given locus favors different alleles in males and females, placing a fundamental constraint on adaptation. However, the relative impact of IaSC on adaptation may become reduced in stressful environments that expose conditionally deleterious mutations to selection. The genetic correlation for fitness between males and females (r(MF)) provides a quantification of IaSC across the genome. We compared IaSC at a benign (29 degrees C) and a stressful (36 degrees C) temperature by estimating r(MF)s in two natural populations of the seed beetle Callosobruchus maculatus using isofemale lines. In one population, we found substantial IaSC under benign conditions signified by a negative r(MF) (-0.51) and, as predicted, a significant reduction of IaSC under stress signified by a reversed and positive r(MF) (0.21). The other population displayed low IaSC at both temperatures (r(MF): 0.38; 0.40). In both populations, isofemale lines harboring alleles beneficial to males but detrimental to females at benign conditions tended to show overall low fitness under stress. These results offer support for low IaSC under stress and suggest that environmentally sensitive and conditionally deleterious alleles that are sexually selected in males mediate changes in IaSC. We discuss implications for adaptive evolution in sexually reproducing populations.

  • 6.
    Berger, David
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    You, Tao
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Minano, Maravillas R.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Grieshop, Karl
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Lind, Martin I.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Arnqvist, Göran
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Maklakov, Alexei A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Sexually antagonistic selection on genetic variation underlying both male and female same-sex sexual behavior2016In: BMC Evolutionary Biology, ISSN 1471-2148, E-ISSN 1471-2148, Vol. 16, article id 88Article in journal (Refereed)
    Abstract [en]

    Background: Intralocus sexual conflict, arising from selection for different alleles at the same locus in males and females, imposes a constraint on sex-specific adaptation. Intralocus sexual conflict can be alleviated by the evolution of sex-limited genetic architectures and phenotypic expression, but pleiotropic constraints may hinder this process. Here, we explored putative intralocus sexual conflict and genetic (co)variance in a poorly understood behavior with near male-limited expression. Same-sex sexual behaviors (SSBs) generally do not conform to classic evolutionary models of adaptation but are common in male animals and have been hypothesized to result from perception errors and selection for high male mating rates. However, perspectives incorporating sex-specific selection on genes shared by males and females to explain the expression and evolution of SSBs have largely been neglected.

    Results: We performed two parallel sex-limited artificial selection experiments on SSB in male and female seed beetles, followed by sex-specific assays of locomotor activity and male sex recognition (two traits hypothesized to be functionally related to SSB) and adult reproductive success (allowing us to assess fitness consequences of genetic variance in SSB and its correlated components). Our experiments reveal both shared and sex-limited genetic variance for SSB. Strikingly, genetically correlated responses in locomotor activity and male sex-recognition were associated with sexually antagonistic fitness effects, but these effects differed qualitatively between male and female selection lines, implicating intralocus sexual conflict at both male-and female-specific genetic components underlying SSB.

    Conclusions: Our study provides experimental support for the hypothesis that widespread pleiotropy generates pervasive intralocus sexual conflict governing the expression of SSBs, suggesting that SSB in one sex can occur due to the expression of genes that carry benefits in the other sex.

  • 7.
    Bilde, T.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Friberg, Urban
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Maklakov, A. A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Fry, J. D.
    Arnqvist, Göran
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    The genetic architecture of fitness in a seed beetle: assessing the potential for indirect genetic benefits of female choice2008In: BMC Evolutionary Biology, ISSN 1471-2148, E-ISSN 1471-2148, Vol. 8, p. 295-Article in journal (Refereed)
    Abstract [en]

    Background: Quantifying the amount of standing genetic variation in fitness represents an empirical challenge. Unfortunately, the shortage of detailed studies of the genetic architecture of fitness has hampered progress in several domains of evolutionary biology. One such area is the study of sexual selection. In particular, the evolution of adaptive female choice by indirect genetic benefits relies on the presence of genetic variation for fitness. Female choice by genetic benefits fall broadly into good genes (additive) models and compatibility (non-additive) models where the strength of selection is dictated by the genetic architecture of fitness. To characterize the genetic architecture of fitness, we employed a quantitative genetic design (the diallel cross) in a population of the seed beetle Callosobruchus maculatus, which is known to exhibit post-copulatory female choice. From reciprocal crosses of inbred lines, we assayed egg production, egg-to-adult survival, and lifetime offspring production of the outbred F1 daughters (F1 productivity). Results: We used the bio model to estimate six components of genetic and environmental variance in fitness. We found sizeable additive and non-additive genetic variance in F-1 productivity, but lower genetic variance in egg-to-adult survival, which was strongly influenced by maternal and paternal effects. Conclusion: Our results show that, in order to gain a relevant understanding of the genetic architecture of fitness, measures of offspring fitness should be inclusive and should include quantifications of offspring reproductive success. We note that our estimate of additive genetic variance in F-1 productivity (CVA = 14%) is sufficient to generate indirect selection on female choice. However, our results also show that the major determinant of offspring fitness is the genetic interaction between parental genomes, as indicated by large amounts of non-additive genetic variance (dominance and/or epistasis) for F-1 productivity. We discuss the processes that may maintain additive and non-additive genetic variance for fitness and how these relate to indirect selection for female choice.

  • 8.
    Bilde, Trine
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    Coates, K.S.
    Birkhofer, K.
    Bird, T.
    Maklakov, Alexei
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    Lubin, Y.
    Aviles, L.
    Survival benefits select for group living in a social spider despite reproductive costs2007In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 20, no 6, p. 2412-2426Article in journal (Refereed)
    Abstract [en]

    The evolution of cooperation requires benefits of group living to exceed costs. Hence, some components of fitness are expected to increase with increasing group size, whereas others may decrease because of competition among group members. The social spiders provide an excellent system to investigate the costs and benefits of group living: they occur in groups of various sizes and individuals are relatively short-lived, therefore life history traits and Lifetime Reproductive Success (LRS) can be estimated as a function of group size. Sociality in spiders has originated repeatedly in phylogenetically distant families and appears to be accompanied by a transition to a system of continuous intra-colony mating and extreme inbreeding. The benefits of group living in such systems should therefore be substantial. We investigated the effect of group size on fitness components of reproduction and survival in the social spider Stegodyphus dumicola in two populations in Namibia. In both populations, the major benefit of group living was improved survival of colonies and late-instar juveniles with increasing colony size. By contrast, female fecundity, female body size and early juvenile survival decreased with increasing group size. Mean individual fitness, estimated as LRS and calculated from five components of reproduction and survival, was maximized for intermediate- to large-sized colonies. Group living in these spiders thus entails a net reproductive cost, presumably because of an increase in intra-colony competition with group size. This cost is traded off against survival benefits at the colony level, which appear to be the major factor favouring group living. In the field, many colonies occur at smaller size than expected from the fitness curve, suggesting ecological or life history constraints on colony persistence which results in a transient population of relatively small colonies.

  • 9.
    Bilde, Trine
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    Maklakov, Alexei A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    Meisner, Katrine
    la Guardia, Lucia
    Friberg, Urban
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    Sex differences in the genetic architecture of lifespan in a seed beetle: extreme inbreeding extends male lifespan2009In: BMC Evolutionary Biology, ISSN 1471-2148, E-ISSN 1471-2148, Vol. 9, p. 33-Article in journal (Refereed)
    Abstract [en]

    Background: Sex differences in lifespan are ubiquitous throughout the animal kingdom but the causes underlying this phenomenon remain poorly understood. Several explanations based on asymmetrical inheritance patterns (sex chromosomes or mitochondrial DNA) have been proposed, but these ideas have rarely been tested experimentally. Alternatively, sexual dimorphism in lifespan could result from sex-specific selection, caused by fundamental differences in how males and females optimize their fitness by allocating resources into current and future reproduction. Results: Here we used sex-specific responses to inbreeding to study the genetic architecture of lifespan and mortality rates in Callosobruchus maculatus, a seed beetle that shows sexual dimorphism in lifespan. Two independent assays revealed opposing sex-specific responses to inbreeding. The combined data set showed that inbred males live longer than outbred males, while females show the opposite pattern. Both sexes suffered reduced fitness measured as lifetime reproductive success as a result of inbreeding. Conclusion: No model based on asymmetrical inheritance can explain increased male lifespan in response to inbreeding. Our results are however compatible with models based on sex-specific selection on reproductive strategies. We therefore suggest that sex-specific differences in lifespan in this species primarily result from sexually divergent selection.

  • 10.
    Bilde, Trine
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    Maklakov, Alexei
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    Schilling, N.
    Inbreeding avoidance in spiders: Evidence for rescue effect in fecundity of female spiders with outbreeding opportunity2007In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 20, no 3, p. 1237-1242Article in journal (Refereed)
    Abstract [en]

    Selection by inbreeding depression should favour mating biases that reduce the risk of fertilization by related mates. However, equivocal evidence for inbreeding avoidance questions the strength of inbreeding depression as a selective force in the evolution of mating biases. Lack of inbreeding avoidance can be because of low risk of inbreeding, variation in tolerance to inbreeding or high costs of outbreeding. We examined the relationship between inbreeding depression and inbreeding avoidance adaptations under two levels of inbreeding in the spider Oedothorax apicatus, asking whether preference for unrelated sperm via pre- and/or post-copulatory mechanisms could restore female fitness when inbreeding depression increases. Using inbred isofemale lines we provided female spiders with one or two male spiders of different relatedness in five combinations: one male sib; one male nonsib; two male sibs; two male nonsibs; one male sib and one male nonsib. We assessed the effect of mating treatment on fecundity and hatching success of eggs after one and three generations of inbreeding. Inbreeding depression in F1 was not sufficient to detect inbreeding avoidance. In F3, inbreeding depression caused a major decline in fecundity and hatching rates of eggs. This effect was mitigated by complete recovery in fecundity in the sib-nonsib treatment, whereas no rescue effect was detected in the hatching success of eggs. The rescue effect is best explained by post-mating discrimination against kin via differential allocation of resources. The natural history of O. apicatus suggests that the costs of outbreeding may be low which combined with high costs of inbreeding should select for avoidance mechanisms. Direct benefits of post-mating inbreeding avoidance and possibly low costs of female multiple mating can favour polyandry as an inbreeding avoidance mechanism.

  • 11.
    Bolund, Elisabeth
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Lummaa, Virpi
    Univ Turku, Dept Biol, FIN-20014 Turku, Finland.;Univ Sheffield, Dept Anim & Plant Sci, Sheffield S10 2TN, S Yorkshire, England..
    Smith, Ken R.
    Univ Utah, Huntsman Canc Inst, Dept Family & Consumer Studies & Populat Sci, Salt Lake City, UT 84112 USA..
    Hanson, Heidi A.
    Univ Utah, Huntsman Canc Inst, Dept Family & Prevent Med & Populat Sci, Salt Lake City, UT 84112 USA..
    Maklakov, Alexei A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Reduced costs of reproduction in females mediate a shift from a male-biased to a female-biased lifespan in humans2016In: Scientific Reports, ISSN 2045-2322, E-ISSN 2045-2322, Vol. 6, article id 24672Article in journal (Refereed)
    Abstract [en]

    The causes underlying sex differences in lifespan are strongly debated. While females commonly outlive males in humans, this is generally less pronounced in societies before the demographic transition to low mortality and fertility rates. Life-history theory suggests that reduced reproduction should benefit female lifespan when females pay higher costs of reproduction than males. Using unique longitudinal demographic records on 140,600 reproducing individuals from the Utah Population Database, we demonstrate a shift from male-biased to female-biased adult lifespans in individuals born before versus during the demographic transition. Only women paid a cost of reproduction in terms of shortened post-reproductive lifespan at high parities. Therefore, as fertility decreased over time, female lifespan increased, while male lifespan remained largely stable, supporting the theory that differential costs of reproduction in the two sexes result in the shifting patterns of sex differences in lifespan across human populations. Further, our results have important implications for demographic forecasts in human populations and advance our understanding of lifespan evolution.

  • 12. Brooks, Robert
    et al.
    Maklakov, Alexei
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    Sex Differences in Obesity Associated with Total Fertility Rate2010In: PLOS ONE, ISSN 1932-6203, Vol. 5, no 5, p. e10587-Article in journal (Refereed)
    Abstract [en]

    The identification of biological and ecological factors that contribute to obesity may help in combating the spreading obesity crisis. Sex differences in obesity rates are particularly poorly understood. Here we show that the strong female bias in obesity in many countries is associated with high total fertility rate, which is well known to be correlated with factors such as low average income, infant mortality and female education. We also document effects of reduced access to contraception and increased inequality of income among households on obesity rates. These results are consistent with studies that implicate reproduction as a risk factor for obesity in women and that suggest the effects of reproduction interact with socioeconomic and educational factors. We discuss our results in the light of recent research in dietary ecology and the suggestion that insulin resistance during pregnancy is due to historic adaptation to protect the developing foetus during famine. Increased access to contraception and education in countries with high total fertility rate might have the additional benefit of reducing the rates of obesity in women.

  • 13. Brooks, Robert
    et al.
    Scott, Isabel M.
    Maklakov, Alexei A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Kasumovic, Michael M.
    Clark, Andrew P.
    Penton-Voak, Ian S.
    National income inequality predicts women's preferences for masculinized faces better than health does2011In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 278, no 1707, p. 810-812Article in journal (Other academic)
  • 14.
    Burgevin, Lorraine
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Friberg, Urban
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Maklakov, Alexei A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Intersexual correlation for same-sex sexual behaviour in an insect2013In: Animal Behaviour, ISSN 0003-3472, E-ISSN 1095-8282, Vol. 85, no 4, p. 759-762Article in journal (Refereed)
    Abstract [en]

    Same-sex sexual behaviour is widespread across taxa and is particularly common in insects, in which up to 50% of copulation attempts by males are directed towards other males in some species. Research effort has focused on male-male same-sex behaviour and the prevailing theory is that benefits of high mating rate combined with poor sex discrimination explain the high incidence of male-male mounting. However, the evolution of female-female mounting is more enigmatic, since females typically do not mount males in order to mate. Using a full-sib design, we found an intersexual correlation for same-sex mounting in the beetle Callosobruchus maculatus. Variation in male-male mounting across families explained over 20% of variation in female-female mounting. Moreover, we found no evidence that same-sex behaviour was related to general activity level in either sex or carried a fitness cost to females. Taken together, our results suggest that female-female mounting is a relatively low-cost behaviour that may be maintained in the population via selection on males.

  • 15. Cayetano, Luis
    et al.
    Maklakov, Alexei A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Brooks, Robert C.
    Bonduriansky, Russell
    Evolution of male and female genitalia following release from sexual selection2011In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 65, no 8, p. 2171-2183Article in journal (Refereed)
    Abstract [en]

    Despite the key functions of the genitalia in sexual interactions and fertilization, the role of sexual selection and conflict in shaping genital traits remains poorly understood. Seed beetle (Callosobruchus maculatus) males possess spines on the intromittent organ, and females possess a thickened reproductive tract wall that also bears spines. We investigated the role of sexual selection and conflict by imposing monogamous mating on eight replicate populations of this naturally polygamous insect, while maintaining eight other populations under polygamy. To establish whether responses to mating system manipulation were robust to ecological context, we simultaneously manipulated life-history selection (early/late reproduction). Over 18-21 generations, male genital spines evolved relatively reduced length in large males (i.e., shallower static allometry) in monogamous populations. Two nonintromittent male genital appendages also evolved in response to the interaction of mating system and ecology. In contrast, no detectable evolution occurred in female genitalia, consistent with the expectation of a delayed response in defensive traits. Our results support a sexually antagonistic role for the male genital spines, and demonstrate the evolution of static allometry in response to variation in sexual selection opportunity. We argue that further advances in the study of genital coevolution will require a much more detailed understanding of the functions of male and female genital traits.

  • 16.
    Chen, Hwei -Yen
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Spagopoulou, Foteini
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Maklakov, Alexei A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Evolution of male age-specific reproduction under differential risks and causes of death: males pay the cost of high female fitness2016In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 29, no 4, p. 848-856Article in journal (Refereed)
    Abstract [en]

    Classic theories of ageing evolution predict that increased extrinsic mortality due to an environmental hazard selects for increased early reproduction, rapid ageing and short intrinsic lifespan. Conversely, emerging theory maintains that when ageing increases susceptibility to an environmental hazard, increased mortality due to this hazard can select against ageing in physiological condition and prolong intrinsic lifespan. However, evolution of slow ageing under high-condition-dependent mortality is expected to result from reallocation of resources to different traits and such reallocation may be hampered by sex-specific trade-offs. Because same life-history trait values often have different fitness consequences in males and females, sexually antagonistic selection can preserve genetic variance for lifespan and ageing. We previously showed that increased condition-dependent mortality caused by heat shock leads to evolution of long-life, decelerated late-life mortality in both sexes and increased female fecundity in the nematode, Caenorhabditis remanei. Here, we used these cryopreserved lines to show that males evolving under heat shock suffered from reduced early-life and net reproduction, while mortality rate had no effect. Our results suggest that heat-shock resistance and associated long-life trade-off with male, but not female, reproduction and therefore sexually antagonistic selection contributes to maintenance of genetic variation for lifespan and fitness in this population.

  • 17.
    Chen, Hwei-Yen
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Maklakov, Alexei
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Longer life span evolves under high rates of condition-dependent mortality2012In: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 22, no 22, p. 2140-2143Article in journal (Refereed)
    Abstract [en]

    Aging affects nearly all organisms, but how aging evolves is still unclear [1-5]. The central prediction of classic theory is that high extrinsic mortality leads to accelerated aging and shorter intrinsic life span [6, 7]. However, this prediction considers mortality as a random process, whereas mortality in nature is likely to be condition dependent. Therefore, the novel theory maintains that condition dependence may dramatically alter, and even reverse, the classic pattern [2-4]. We present experimental evidence for the evolution of longer life span under high condition-dependent mortality. We employed an experimental evolution design, using a nematode, Caenorhabditis remanei, that allowed us to disentangle the effects of mortality rate (high versus low) and mortality source (random versus condition dependent). We observed the evolution of shorter life span under high random mortality, confirming the classic prediction. In contrast, high condition-dependent mortality led to the evolution of longer life span, supporting a key role of condition dependence in the evolution of aging. This life-span extension was not the result of a trade-off with reproduction. By simultaneously corroborating the classic results [8-10] and providing the first experimental evidence for the novel theory [2-4], our study resolves apparent contradictions in the study of aging and challenges the traditional paradigm by demonstrating that condition-environment interactions dictate the evolutionary trajectory of aging.

  • 18.
    Chen, Hwei-yen
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Maklakov, Alexei A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Condition dependence of male mortality drives the evolution of sex differences in longevity2014In: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 24, no 20, p. 2423-2427Article in journal (Refereed)
    Abstract [en]

    Males and females age at different rates and have different life expectancies across the animal kingdom, but what causes the longevity "gender gaps" remains one of the most fiercely debated puzzles among biologists and demographers [1-7]. Classic theory predicts that the sex experiencing higher rate of extrinsic mortality evolves faster aging and reduced longevity [1]. However, condition dependence of mortality [8, 9] can counter this effect by selecting against senescence in whole-organism performance [5, 10]. Contrary to the prevailing view but in line with an emerging new theory [7-9, 11], we show that the evolution of sex difference in longevity depends on the factors that cause sex-specific mortality and cannot be predicted from the mortality rate alone. Experimental evolution in an obligately sexual roundworm, Caenorhabditis remanei, in which males live longer than females, reveals that sexual dimorphism in longevity erodes rapidly when the extrinsic mortality in males is increased at random. We thus experimentally demonstrate evolution of the sexual monomorphism in longevity in a sexually dimorphic organism. Strikingly, when extrinsic mortalityis increased in a way that favors survival of fast-moving individuals, males evolve increased longevities, thereby widening the gender gap. Thus,sex-specific selection on whole-organism performance in males renders them less prone to the ravages of old age than females, despite higher rates of extrinsic mortality. Our results reconcile previous research with recent theoretical breakthroughs [8, 9] by showing that sexual dimorphism inlongevity evolves rapidly and predictably as a result of the sex-specific interactions between environmental hazard and organism's condition.

  • 19.
    Chen, Hwei-yen
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Maklakov, Alexei A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    The worm that lived: evolution of rapid aging under high extrinsic mortality revisited2013In: Worm, Vol. 2, no 3, article id e23704Article in journal (Refereed)
    Abstract [en]

    Organisms age because of the “selection shadow”—the decline of the force of natural selection with age. Seemingly straightforward corollary of this theory is the Medawar-Williams prediction, which maintains that increased extrinsic (non-aging) mortality will result in the evolution of accelerated aging and decreased longevity. Despite its centrality to modern thinking about the ultimate causes of aging, this prediction ignores the fact that mortality is often a non-random process depending on individual condition. Increased condition-dependent mortality inescapably results in increased selection for resistance against the agent of mortality. Provided that resistance to various stressors is commonly associated with increased longevity, the evolutionary outcome is no longer certain. We recently documented this experimentally by showing that populations of Caenorhabditis remanei evolved to live shorter under high extrinsic mortality, but only when mortality was applied haphazardly. On the contrary, when extrinsic mortality was caused by heat-shock, populations experiencing the same rate of increased mortality evolved greater longevities, notwithstanding increased “selection shadow.” Intriguingly, stress-resistant and long-lived worms were also more fecund. We discuss these results in the light of recent theoretical developments, such as condition-environment interactions and hyperfunction theory of aging.

  • 20.
    Chen, Hwei-yen
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Zajitschek, Felix
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Maklakov, Alexei A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Why ageing stops: heterogeneity explains late-life mortality deceleration in nematodes2013In: Biology Letters, ISSN 1744-9561, E-ISSN 1744-957X, Vol. 9, no 5, p. 20130217-Article in journal (Refereed)
    Abstract [en]

    While ageing is commonly associated with exponential increase in mortality with age, mortality rates paradoxically decelerate late in life resulting in distinct mortality plateaus. Late-life mortality plateaus have been discovered in a broad variety of taxa, including humans, but their origin is hotly debated. One hypothesis argues that deceleration occurs because the individual probability of death stops increasing at very old ages, predicting the evolution of earlier onset of mortality plateaus under increased rate of extrinsic mortality. By contrast, heterogeneity theory suggests that mortality deceleration arises from individual differences in intrinsic lifelong robustness and predicts that variation in robustness between populations will result in differences in mortality deceleration. We used experimental evolution to directly test these predictions by independently manipulating extrinsic mortality rate (high or low) and mortality source (random death or condition-dependent) to create replicate populations of nematodes, Caenorhabditis remanei that differ in the strength of selection in late-life and in the level of lifelong robustness. Late-life mortality deceleration evolved in response to differences in mortality source when mortality rate was held constant, while there was no consistent response to differences in mortality rate. These results provide direct experimental support for the heterogeneity theory of late-life mortality deceleration.

  • 21. Dowling, D. K.
    et al.
    Maklakov, A. A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Friberg, U.
    Hailer, F.
    Applying the genetic theories of ageing to the cytoplasm: cytoplasmic genetic covariation for fitness and lifespan2009In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 22, no 4, p. 818-827Article in journal (Refereed)
    Abstract [en]

    Two genetic models exist to explain the evolution of ageing - mutation accumulation (MA) and antagonistic pleiotropy (AP). Under MA, a reduced intensity of selection with age results in accumulation of late-acting deleterious mutations. Under AP, late-acting deleterious mutations accumulate because they confer beneficial effects early in life. Recent studies suggest that the mitochondrial genome is a major player in ageing. It therefore seems plausible that the MA and AP models will be relevant to genomes within the cytoplasm. This possibility has not been considered previously. We explore whether patterns of covariation between fitness and ageing across 25 cytoplasmic lines, sampled from a population of Drosophila melanogaster, are consistent with the genetic associations predicted under MA or AP. We find negative covariation for fitness and the rate of ageing, and positive covariation for fitness and lifespan. Notably, the direction of these associations is opposite to that typically predicted under AP.

  • 22.
    Erkosar, Berra
    et al.
    Univ Lausanne, Dept Ecol & Evolut, Lausanne, Switzerland.;Univ Lausanne, Dept Fundamental Microbiol, Lausanne, Switzerland..
    Yashiro, Erika
    Univ Lausanne, Dept Fundamental Microbiol, Lausanne, Switzerland..
    Zajitschek, Felix
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. Univ New South Wales, Sch Biol Earth & Environm Sci, Evolut & Ecol Res Ctr, Sydney, NSW, Australia..
    Friberg, Urban
    Linkoping Univ, AVIAN Behav Genom & Physiol Grp, IFM Biol, Linkoping, Sweden..
    Maklakov, Alex A
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    van der Meer, Jan R.
    Univ Lausanne, Dept Fundamental Microbiol, Lausanne, Switzerland..
    Kawecki, Tadeusz J.
    Univ Lausanne, Dept Ecol & Evolut, Lausanne, Switzerland..
    Host diet mediates a negative relationship between abundance and diversity of Drosophila gut microbiota2018In: Ecology and Evolution, ISSN 2045-7758, E-ISSN 2045-7758, Vol. 8, no 18, p. 9491-9502Article in journal (Refereed)
    Abstract [en]

    Nutrient supply to ecosystems has major effects on ecological diversity, but it is unclear to what degree the shape of this relationship is general versus dependent on the specific environment or community. Although the diet composition in terms of the source or proportions of different nutrient types is known to affect gut microbiota composition, the relationship between the quantity of nutrients supplied and the abundance and diversity of the intestinal microbial community remains to be elucidated. Here, we address this relationship using replicate populations of Drosophila melanogaster maintained over multiple generations on three diets differing in the concentration of yeast (the only source of most nutrients). While a 6.5-fold increase in yeast concentration led to a 100-fold increase in the total abundance of gut microbes, it caused a major decrease in their alpha diversity (by 45-60% depending on the diversity measure). This was accompanied by only minor shifts in the taxonomic affiliation of the most common operational taxonomic units (OTUs). Thus, nutrient concentration in host diet mediates a strong negative relationship between the nutrient abundance and microbial diversity in the Drosophila gut ecosystem.

  • 23.
    Fricke, Claudia
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    Maklakov, Alexei A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    Male age does not affect female fitness in a polyandrous beetle, Callosobruchus maculatus2007In: Animal Behaviour, ISSN 0003-3472, E-ISSN 1095-8282, Vol. 74, no 3, p. 541-548Article in journal (Refereed)
    Abstract [en]

    Males in different taxa are likely to suffer from a reduction in the quantity and/or quality of their sperm with age. This predicts age-related direct and indirect effects on female fitness. Hence, females may be selected to avoid matings with old males, or to employ alternative mating tactics, such as polyandry, to avoid fertilization by sperm of older males. In contrast, ‘viability indicator’ models of mate choice predict female preference for old males that have proven their survival ability and signal more reliably. We used a polygamous seed beetle, Callosobruchus maculatus, to test for the effects of male age on male mating success and examine the relationship between male age and female fitness, measured as female life span, lifetime fecundity, hatching success of eggs, larval development rate and egg-to-adult survival of offspring. Furthermore, we tested the hypothesis that polyandry may protect females against low numbers of functional sperm produced by old males. We report, contrary to previous findings, that male mating success indeed decreases with male age in this species. However, mating with older males did not in any way compromise female fitness and, consequently, we found no support for the idea that polyandry helps females reduce any costs of mating with older males.

  • 24.
    Griffin, Robert M.
    et al.
    Univ Turku, Dept Biol, Turku 20014, Finland..
    Hayward, Adam D.
    Univ Stirling, Dept Biol & Environm Sci, Stirling FK9 4LA, Scotland..
    Bolund, Elisabeth
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Maklakov, Alex A
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. Univ East Anglia, Sch Biol Sci, Norwich Res Pk, Norwich NR4 7TJ, Norfolk, England..
    Lummaa, Virpi
    Univ Turku, Dept Biol, Turku 20014, Finland..
    Sex differences in adult mortality rate mediated by early-life environmental conditions2018In: Ecology Letters, ISSN 1461-023X, E-ISSN 1461-0248, Vol. 21, no 2, p. 235-242Article in journal (Refereed)
    Abstract [en]

    Variation in sex differences is affected by both genetic and environmental variation, with rapid change in sex differences being more likely due to environmental change. One case of rapid change in sex differences is human lifespan, which has become increasingly female-biased in recent centuries. Long-term consequences of variation in the early-life environment may, in part, explain such variation in sex differences, but whether the early-life environment mediates sex differences in life-history traits is poorly understood in animals. Combining longitudinal data on 60 cohorts of pre-industrial Finns with environmental data, we show that the early-life environment is associated with sex differences in adult mortality and expected lifespan. Specifically, low infant survival rates and high rye yields (an important food source) in early-life are associated with female-bias in adult lifespan. These results support the hypothesis that environmental change has the potential to affect sex differences in life-history traits in natural populations of long-lived mammals.

  • 25.
    Hooper, Amy K.
    et al.
    Univ New South Wales, Evolut & Ecol Res Ctr, Sch Biol Earth & Environm Sci, Sydney, NSW 2052, Australia..
    Spagopoulou, Foteini
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Wylde, Zachariah
    Univ New South Wales, Evolut & Ecol Res Ctr, Sch Biol Earth & Environm Sci, Sydney, NSW 2052, Australia..
    Maklakov, Alexei A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Bonduriansky, Russell
    Univ New South Wales, Evolut & Ecol Res Ctr, Sch Biol Earth & Environm Sci, Sydney, NSW 2052, Australia..
    Ontogenetic timing as a condition-dependent life history trait: High-condition males develop quickly, peak early, and age fast2017In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 71, no 3, p. 671-685Article in journal (Refereed)
    Abstract [en]

    Within-population variation in ageing remains poorly understood. In males, condition-dependent investment in secondary sexual traits may incur costs that limit ability to invest in somatic maintenance. Moreover, males often express morphological and behavioral secondary sexual traits simultaneously, but the relative effects on ageing of investment in these traits remain unclear. We investigated the condition dependence of male life history in the neriid fly Telostylinus angusticollis. Using a fully factorial design, we manipulated male early-life condition by varying nutrient content of the larval diet and, subsequently, manipulated opportunity for adult males to interact with rival males. We found that high-condition males developed more quickly and reached their reproductive peak earlier in life, but also experienced faster reproductive ageing and died sooner than low-condition males. By contrast, interactions with rival males reduced male lifespan but did not affect male reproductive ageing. High-condition in early life is therefore associated with rapid ageing in T. angusticollis males, even in the absence of damaging male-male interactions. Our results show that abundant resources during the juvenile phase are used to expedite growth and development and enhance early-life reproductive performance at the expense of late-life performance and survival, demonstrating a clear link between male condition and ageing.

  • 26.
    Kotrschal, Alexander
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Corral-Lopez, A.
    Zajitschek, Susanne
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Immler, Simone
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Maklakov, Alexei A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Kolm, Niclas
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Positive genetic correlation between brain size and sexual traits in male guppies artificially selected for brain size2015In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 28, no 4, p. 841-850Article in journal (Refereed)
    Abstract [en]

    Brain size is an energetically costly trait to develop and maintain. Investments into other costly aspects of an organism's biology may therefore place important constraints on brain size evolution. Sexual traits are often costly and could therefore be traded off against neural investment. However, brain size may itself be under sexual selection through mate choice on cognitive ability. Here, we use guppy (Poecilia reticulata) lines selected for large and small brain size relative to body size to investigate the relationship between brain size, a large suite of male primary and secondary sexual traits, and body condition index. We found no evidence for trade-offs between brain size and sexual traits. Instead, larger-brained males had higher expression of several primary and precopulatory sexual traits - they had longer genitalia, were more colourful and developed longer tails than smaller-brained males. Larger-brained males were also in better body condition when housed in single-sex groups. There was no difference in post-copulatory sexual traits between males from the large- and small-brained lines. Our data do not support the hypothesis that investment into sexual traits is an important limiting factor to brain size evolution, but instead suggest that brain size and several sexual traits are positively genetically correlated.

  • 27.
    Kotrschal, Alexander
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Lievens, Eva J. P.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Dahlbom, Josefin
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience.
    Bundsen, Andreas
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Semenova, Svetlana
    Sundvik, Maria
    Maklakov, Alexei A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Winberg, Svante
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Neuroscience, Physiology.
    Panula, Pertti
    Kolm, Niclas
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Artificial Selection on Relative Brain Size Reveals a Positive Genetic Correlation Between Brain Size and Proactive Personality in the Guppy2014In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 68, no 4, p. 1139-1149Article in journal (Refereed)
    Abstract [en]

    Animal personalities range from individuals that are shy, cautious, and easily stressed (a "reactive" personality type) to individuals that are bold, innovative, and quick to learn novel tasks, but also prone to routine formation (a "proactive" personality type). Although personality differences should have important consequences for fitness, their underlying mechanisms remain poorly understood. Here, we investigated how genetic variation in brain size affects personality. We put selection lines of large- and small-brained guppies (Poecilia reticulata), with known differences in cognitive ability, through three standard personality assays. First, we found that large-brained animals were faster to habituate to, and more exploratory in, open field tests. Large-brained females were also bolder. Second, large-brained animals excreted less cortisol in a stressful situation (confinement). Third, large-brained animals were slower to feed from a novel food source, which we interpret as being caused by reduced behavioral flexibility rather than lack of innovation in the large-brained lines. Overall, the results point toward a more proactive personality type in large-brained animals. Thus, this study provides the first experimental evidence linking brain size and personality, an interaction that may affect important fitness-related aspects of ecology such as dispersal and niche exploration.

  • 28.
    Kotrschal, Alexander
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Rogell, Björn
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Bundsen, Andreas
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Svensson, Beatrice
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Zajitschek, Susanne
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Brännström, Ioana
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Immler, Simone
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Maklakov, Alexei A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Kolm, Niclas
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    The benefit of evolving a larger brain: big-brained guppies perform better in a cognitive task2013In: Animal Behaviour, ISSN 0003-3472, E-ISSN 1095-8282, Vol. 86, no 4, p. E4-E6Article in journal (Refereed)
  • 29.
    Kotrschal, Alexander
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Rogell, Björn
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Bundsen, Andreas
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Svensson, Beatrice
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Zajitschek, Susanne
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Brännström, Ioana Onut
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Immler, Simone
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Maklakov, Alexei A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Kolm, Niclas
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Artificial selection on relative brain size in the guppy reveals costs and benefits of evolving a larger brain2013In: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 23, no 2, p. 168-171Article in journal (Refereed)
    Abstract [en]

    The large variation in brain size that exists in the animal kingdom has been suggested to have evolved through the balance between selective advantages of greater cognitive ability and the prohibitively high energy demands of a larger brain (the "expensive-tissue hypothesis" [1]). Despite over a century of research on the evolution of brain size, empirical support for the trade-off between cognitive ability and energetic costs is based exclusively on correlative evidence [2], and the theory remains controversial [3, 4]. Here we provide experimental evidence for costs and benefits of increased brain size. We used artificial selection for large and small brain size relative to body size in a live-bearing fish, the guppy (Poecilia reticulata), and found that relative brain size evolved rapidly in response to divergent selection in both sexes. Large-brained females outperformed small-brained females in a numerical learning assay designed to test cognitive ability. Moreover, large-brained lines, especially males, developed smaller guts, as predicted by the expensive-tissue hypothesis [1], and produced fewer offspring. We propose that the evolution of brain size is mediated by a functional trade-off between increased cognitive ability and reproductive performance and discuss the implications of these findings for vertebrate brain evolution.

  • 30.
    Kotrschal, Alexander
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Rogell, Björn
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Maklakov, Alexei A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Kolm, Nichlas
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Sex-specific plasticity in brain morphology depends on social environment of the guppy, Poecilia reticulata2012In: Behavioral Ecology and Sociobiology, ISSN 0340-5443, E-ISSN 1432-0762, Vol. 66, no 11, p. 1485-1492Article in journal (Refereed)
    Abstract [en]

    The vertebrate brain is a remarkably plastic organ, which responds quickly to environmental changes. However, to date, studies investigating plasticity in brain morphology have focused mostly on the physical properties of the surrounding environment, and little is known about brain plasticity in response to the social environment. Moreover, sex differences in brain plasticity remain virtually unexplored. Here, we tested how the social environment influenced brain morphology in adult males and females using experimental manipulation of the sex composition of social pairs (same sex vs. mixed sex) in the guppy (Poecilia reticulata). We detected substantial sex-specific plasticity in both the overall brain size (controlling for body size) and separate brain structures. The brain size was larger in males that interacted with females, and female optic tectum was larger in female-only groups. Overall, females had larger olfactory bulbs and cerebellum in comparison to males. While net sexual dimorphism in the brain structure can be explained in light of the known differences in boldness and foraging behaviour between the sexes, our results also support that cognitive demands associated with courtship behaviour can lead to plastic changes in the brain size. Our findings demonstrate that not only social environment can generate rapid, plastic responses in the vertebrate brain but also that such responses can depend strongly on sex.

  • 31.
    Lind, Martin I.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Berg, Elena C.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Alavioon, Ghazal
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Maklakov, Alexei A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Evolution of differential maternal age effects on male and female offspring development and longevity2015In: Functional Ecology, ISSN 0269-8463, E-ISSN 1365-2435, Vol. 29, no 1, p. 104-110Article in journal (Refereed)
    Abstract [en]

    Maternal age effects on life-history traits, including longevity, are widespread and can be seen as a manifestation of ageing. However, little is known about how maternal life span may influence the maternal age effect. At a given chronological age, a long-lived parent may be at a younger biological age than a short-lived parent and thus has a less severe parental age effect. However, earlier work using experimentally evolved short- and long-lived lines did not support this hypothesis. We scored developmental time and longevity of 14995 individual seed beetles, Callosobruchus maculatus derived from replicate short-lived and long-lived lines created via artificial selection on male life span. Offspring from older mothers had shorter life span, which is consistent with most of the literature. We found support for the hypothesis that detrimental maternal age effects evolve to be weaker under selection for long life span. However, this finding was only apparent in males, suggesting that maternal age affects male and female offspring differently. These results suggest that sex-dependent parental age effects should be incorporated in the studies of longevity and ageing evolution and that selection on one sex can cause evolution of parental age effects in the other sex.

  • 32.
    Lind, Martin I.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Chen, Hwei-yen
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Cortazar-Chinarro, Maria
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Maklakov, Alexei A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Rapamycin additively extends lifespan in short- and long-lived lines of the nematode Caenorhabditis remanei2017In: Experimental Gerontology, ISSN 0531-5565, E-ISSN 1873-6815, Vol. 90, p. 79-82Article in journal (Refereed)
    Abstract [en]

    Despite tremendous progress in finding genes that, when manipulated, affects lifespan, little is known about the genetics underlying natural variation in lifespan. While segregating genetic variants for lifespan has been notoriously difficult to find in genome-wide association studies (GWAS), a complementary approach is to manipulate key genetic pathways in lines that differ in lifespan. If these candidate pathways are down regulated in long-lived lines, these lines can be predicted to respond less to pharmaceutical down-regulation of these pathways than short-lived lines. Experimental studies have identified the nutrient-sensing pathway TOR as a key regulator of lifespan in model organisms, and this pathway can effectively be down regulated using the drug rapamycin, which extends lifespan in all tested species. We expose short-and long-lived lines of the nematode Caenorhabditis remanei to rapamycin, and investigate if long-lived lines, which are hypothesized to already have down-regulated TOR signaling, respond less to rapamycin. We found no interaction between line and rapamycin treatment, since rapamycin extended lifespan independent of the intrinsic lifespan of the lines. This shows that rapamycin is equally effective on long and short-lived lines, and suggests that the evolution of long life may involve more factors that down-regulation of TOR.

  • 33.
    Lind, Martin I.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Chen, Hwei-yen
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Meurling, Sara
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Guevara Gil, Anna Cristina
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Carlsson, Hanne
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Zwoinska, Martyna K.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Andersson, Johan
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Larva, Tuuli
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Maklakov, Alexei A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. School of Biological Sciences, University of East Anglia, Norwich, UK.
    Slow development as an evolutionary cost of long life2017In: Functional Ecology, ISSN 0269-8463, E-ISSN 1365-2435, Vol. 31, no 6, p. 1252-1261Article in journal (Refereed)
    Abstract [en]

    Life-history theory predicts a trade-off between early-life fitness and life span. While the focus traditionally has been on the fecundity-life span trade-off, there are strong reasons to expect trade-offs with growth rate and/or development time. We investigated the roles of growth rate and development time in the evolution of life span in two independent selection experiments in the outcrossing nematode Caenorhabditis remanei. First, we found that selection under heat-shock leads to the evolution of increased life span without fecundity costs, but at the cost of slower development. Thereafter, the putative evolutionary links between development time, growth rate, fecundity, heat-shock resistance and life span were independently assessed in the second experiment by directly selecting for fast or slow development. This experiment confirmed our initial findings, since selection for slow development resulted in the evolution of long life span and increased heat-shock resistance. Because there were no consistent trade-offs with growth rate or fecundity, our results highlight the key role of development rate - differentiation of the somatic cells per unit of time - in the evolution of life span. Since development time is under strong selection in nature, reduced somatic maintenance resulting in shorter life span may be a widespread cost of rapid development.

  • 34.
    Lind, Martin I.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Ravindran, Sanjana
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Sekajova, Zuzana
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Carlsson, Hanne
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. Univ East Anglia, Sch Biol Sci, Norwich, Norfolk, England.
    Hinas, Andrea
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology.
    Maklakov, Alex A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. Univ East Anglia, Sch Biol Sci, Norwich, Norfolk, England.
    Experimentally reduced insulin/IGF‐1 signaling in adulthood extends lifespan of parents and improves Darwinian fitness of their offspring2019In: EVOLUTION LETTERS, ISSN 2056-3744, Vol. 3, no 2, p. 207-216Article in journal (Refereed)
    Abstract [en]

    Classical theory maintains that ageing evolves via energy trade-offs between reproduction and survival leading to accumulation of unrepaired cellular damage with age. In contrast, the emerging new theory postulates that ageing evolves because of deleterious late-life hyper-function of reproduction-promoting genes leading to excessive biosynthesis in late-life. The hyper-function theory uniquely predicts that optimizing nutrient-sensing molecular signaling in adulthood can simultaneously postpone ageing and increase Darwinian fitness. Here, we show that reducing evolutionarily conserved insulin/IGF-1 nutrient-sensing signaling via daf-2 RNA interference (RNAi) fulfils this prediction in Caenorhabditis elegans nematodes. Long-lived daf-2 RNAi parents showed normal fecundity as self-fertilizing hermaphrodites and improved late-life reproduction when mated to males. Remarkably, the offspring of daf-2 RNAi parents had higher Darwinian fitness across three different genotypes. Thus, reduced nutrient-sensing signaling in adulthood improves both parental longevity and offspring fitness supporting the emerging view that suboptimal gene expression in late-life lies at the heart of ageing.

  • 35.
    Maklakov, Alex A
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. Univ East Anglia, Sch Biol Sci, Norwich Res Pk, Norwich NR4 7TJ, Norfolk, England..
    Carlsson, Hanne
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Denbaum, Philip
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Lind, Martin I.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Mautz, Brian
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Hinas, Andrea
    Uppsala University, Disciplinary Domain of Medicine and Pharmacy, Faculty of Medicine, Department of Medical Biochemistry and Microbiology.
    Immler, Simone
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology. Univ East Anglia, Sch Biol Sci, Norwich Res Pk, Norwich NR4 7TJ, Norfolk, England..
    Antagonistically pleiotropic allele increases lifespan and late-life reproduction at the cost of early-life reproduction and individual fitness2017In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 284, no 1856, article id 20170376Article in journal (Refereed)
    Abstract [en]

    Evolutionary theory of ageing maintains that increased allocation to early-life reproduction results in reduced somatic maintenance, which is predicted to compromise longevity and late-life reproduction. This prediction has been challenged by the discovery of long-lived mutants with no loss of fecundity. The first such long-lived mutant was found in the nematode worm Caenorhabditis elegans. Specifically, partial loss-of-function mutation in the age-1 gene, involved in the nutrient-sensing insulin/insulin-like growth factor signalling pathway, confers longevity, as well as increased resistance to pathogens and to temperature stress without appreciable fitness detriment. Here, we show that the long-lived age-1(hx546) mutant has reduced fecundity and offspring production in early-life, but increased fecundity, hatching success, and offspring production in late-life compared with wild-type worms under standard conditions. However, reduced early-life performance of long-lived mutant animals was not fully compensated by improved performance in late-life and resulted in reduced individual fitness. These results suggest that the age-1(hx546) allele has opposing effects on early-life versus late-life fitness in accordance with antagonistic pleiotropy (AP) and disposable soma theories of ageing. These findings support the theoretical conjecture that experimental studies based on standing genetic variation underestimate the importance of AP in the evolution of ageing.

  • 36.
    Maklakov, Alex A
    et al.
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology. Zooekologi.
    Kremer, Natasha
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology. Zooekologi.
    Arnqvist, Göran
    Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Teknisk-naturvetenskapliga vetenskapsområdet, Faculty of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    Adaptive male effects on female ageing in seed beetles2005In: Proceedings of the Royal Society London B, Vol. 272, p. 2485-2489Article in journal (Refereed)
  • 37.
    Maklakov, Alexei A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Aging: Why Do Organisms Live Too Long?2013In: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 23, no 22, p. R1003-R1005Article in journal (Other academic)
  • 38.
    Maklakov, Alexei A.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Arnqvist, Göran
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Testing for Direct and Indirect Effects of Mate Choice by Manipulating Female Choosiness2009In: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 19, no 22, p. 1903-1906Article in journal (Refereed)
    Abstract [en]

    Despite a massive research effort, our understanding of the evolution of female mate choice remains incomplete [1, 2]. A central problem is that the predominating empirical research tradition has focused on male traits, yet the key question is whether female choice traits are maintained because of direct effects on female fitness or because of indirect genetic effects in offspring that may be associated with such traits. Here, we address this question by using a novel research strategy that employs experimental phenotypic manipulation of a female choice trait in an insect model system, the seed beetle Callosobruchus chinensis (Coleoptera: Bruchidae). We show that females with increased efficiency of choice enjoy strongly elevated fitness compared to females with reduced choice efficiency. In contrast, we found no effects of female choice efficiency on offspring fitness. Our results show that female choice is maintained by direct selection in females in this system, whereas indirect selection is relatively weak at most. We suggest that phenotypic engineering of female choice traits can greatly advance our ability to elucidate the relative importance of direct and indirect selection for the maintenance of female choice.

  • 39.
    Maklakov, Alexei A.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Cayetano, Luis
    Brooks, Robert C.
    Bonduriansky, Russell
    The roles of life-history selection and sexual selection in the adaptive evolution of mating behavior in a beetle2010In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 64, no 5, p. 1273-1282Article in journal (Refereed)
    Abstract [en]

    Although there is continuing debate about whether sexual selection promotes or impedes adaptation to novel environments, the role of mating behavior in such adaptation remains largely unexplored We investigated the evolution of mating behavior (latency to mating, mating probability and duration) in replicate populations of seed beetles Callosobruchus maculatus subjected to selection on life-history ("Young" vs. "Old" reproduction) under contrasting regimes of sexual selection ("Monogamy" vs. "Polygamy"). Life-history selection is predicted to favor delayed mating in "Old" females, but sexual conflict under polygamy can potentially retard adaptive life-history evolution. We found that life-history selection yielded the predicted changes in mating behavior, but sexual selection regime had no net effect. In within-line crosses, populations selected for late reproduction showed equally reduced early-life mating probability regardless of mating system. In between-line crosses, however, the effect of life-history selection on early-life mating probability was stronger in polygamous lines than in monogamous ones. Thus, although mating system influenced male-female coevolution, removal of sexual selection did not affect the adaptive evolution of mating behavior Importantly, our study shows that the interaction between sexual selection and life-history selection can result in either increased or decreased reproductive divergence depending on the ecological context.

  • 40.
    Maklakov, Alexei A.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Friberg, Urban
    Linköping Univ, IFM Biol AVIAN Behav Genom & Physiol Grp, S-58183 Linköping, Sweden..
    Ageing: Why Males Curtail the Longevity of Their Mates2016In: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 26, no 20, p. R929-R932Article in journal (Other academic)
    Abstract [en]

    Male nematodes secrete pheromones that accelerate the somatic senescence of potential mates. A new study shows that this harm most likely is an unintended by-product of the males' aim to speed up sexual maturation and delay reproductive senescence of future partners.

  • 41.
    Maklakov, Alexei A.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Fricke, Claudia
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution. Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Sexual selection did not contribute to the evolution of male lifespan under curtailed age at reproduction in a seed beetle2009In: Ecological Entomology, ISSN 0307-6946, E-ISSN 1365-2311, Vol. 34, no 5, p. 638-643Article in journal (Refereed)
    Abstract [en]

    1. Sexual selection is a powerful evolutionary force that is hypothesised to play an important role in the evolution of lifespan. Here we test for the potential contribution of sexual selection to the rapid evolution of male lifespan in replicated laboratory populations of the seed beetle, Callosobruchus maculatus. 2. For 35 generations, newly hatched virgin male beetles from eight different populations were allowed to mate for 24 h and then discarded. Sexual selection was removed in half of these populations by enforcing random monogamy. 3. Classic theory predicts that because of sexual competition, males from sexually selected lines would have higher age-specific mortality rates and shorter lifespan than males from monogamous lines. 4. Alternatively, condition-dependent sexual selection may also favour genes that have positive pleiotropic effects on lifespan and ageing. 5. Males from all eight populations evolved shorter lifespans compared with the source population. However, there was no difference in lifespan between males from populations with or without sexual selection. Thus, sexual selection did not contribute to the evolution of male lifespan despite the fact that such evolution did occur in our study populations.

  • 42.
    Maklakov, Alexei A.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    Fricke, Claudia
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    Arnqvist, Göran
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    Sexual selection affects lifespan and aging in the seed beetle2007In: Aging Cell, ISSN 1474-9718, E-ISSN 1474-9726, Vol. 6, no 6, p. 739-744Article in journal (Refereed)
    Abstract [en]

    Sexual selection in general, and sexual conflict in particular, should affect the evolution of lifespan and aging. Using experimental evolution, we tested whether removal of sexual selection leads to the evolution of accelerated or decelerated senescence. We subjected replicated populations of the seed beetle Callosobruchus maculatus to either of two selection regimes for 35 generations. These regimes either allowed (polygamy) or removed the potential (monogamy) for sexual selection to operate. To test for the evolution of intrinsic differences between the two selection regimes, we assayed longevity in replicate cohorts of virgin females and males. Virgin females from populations evolving under sexual selection had reduced lifespan as predicted by the sexual conflict theory of aging. However, this reduction was due to increased baseline mortality rather than an increase in age-specific mortality rates with age. We discuss these findings in light of other data from this model system and suggest that system-specific idiosyncrasies may often modulate the general effects of male-female coevolution on the evolution of aging.

  • 43.
    Maklakov, Alexei A.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Immler, Simone
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    The Expensive Germline and the Evolution of Ageing2016In: Current Biology, ISSN 0960-9822, E-ISSN 1879-0445, Vol. 26, no 13, p. R577-R586Article, review/survey (Refereed)
    Abstract [en]

    The trade-off between survival and reproduction is the bedrock of the evolutionary theory of ageing. The reproductive system regulates ageing of the soma, and removal of germ cells extends somatic lifespan and increases resistance to a broad variety of abiotic and biotic stresses. The general explanation for this somatic response is that reduced reproduction frees up resources for survival. Remarkably, however, the disruption of molecular signaling pathways that regulate ageing increases lifespan without the obligatory reduction in fecundity, thus challenging the key role of the survival-reproduction trade-off. Here, we review the diverse literature on the costs of lifespan extension and suggest that the current paradigm is overly centered on the trade-off between lifespan and fecundity, often neglecting key aspects of fitness, such as development time, defense against parasites and, in particular, the high costs of germline maintenance. Compromised germline maintenance increases germline mutation rate, which reduces offspring fitness and ultimately can terminate germline proliferation across generations. We propose that future work should incorporate the costs of germline maintenance in the study of ageing evolution, as well as in applied biomedical research, by assessing offspring fitness.

  • 44.
    Maklakov, Alexei A.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Immler, Simone
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Gonzalez-Voyer, Alejandro
    Rönn, Johanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Kolm, Niclas
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal Ecology.
    Brains and the city: big-brained passerine birds succeed in urban environments2011In: Biology Letters, ISSN 1744-9561, E-ISSN 1744-957X, Vol. 7, no 5, p. 730-732Article in journal (Refereed)
    Abstract [en]

    Urban regions are among the most human-altered environments on Earth and they are poised for rapid expansion following population growth and migration. Identifying the biological traits that determine which species are likely to succeed in urbanized habitats is important for predicting global trends in biodiversity. We provide the first evidence for the intuitive yet untested hypothesis that relative brain size is a key factor predisposing animals to successful establishment in cities. We apply phylogenetic mixed modelling in a Bayesian framework to show that passerine species that succeed in colonizing at least one of 12 European cities are more likely to belong to big-brained lineages than species avoiding these urban areas. These data support findings linking relative brain size with the ability to persist in novel and changing environments in vertebrate populations, and have important implications for our understanding of recent trends in biodiversity.

  • 45.
    Maklakov, Alexei A.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Immler, Simone
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Gonzalez-Voyer, Alejandro
    Rönn, Johanna
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Kolm, Niclas
    Brains and the city in passerine birds: re-analysis and confirmation of the original result2013In: Biology Letters, ISSN 1744-9561, E-ISSN 1744-957X, Vol. 9, no 6, p. 20130859-Article in journal (Refereed)
    Abstract [en]

    Our original paper [1] included two Bayesian analyses [2] of the association between brain size and the probability of a passerine species of bird breeding in the city centre—at the level of families and at the level of individual species—with both analyses suggesting the same pattern. It has since been brought to our attention that in one of the analyses at the level of individual species, the residual variance was not fixed to 1 resulting in overestimation of the variance. We re-ran the analysis using fixed residual variance and the results support the original conclusion that relative brain size is associated with breeding in the city centre (ln brain size: posterior mean, 324.53, 95% credibility interval, 52.61–601.35; ln body size: posterior mean, −276.22, 95% credibility interval, −490.60 to −70.32). Furthermore, we applied a complimentary approach using logistic regression to test whether brain size predicts breeding in the city centre (yes/no) without accounting for phylogeny. This analysis also resulted in a significant positive association between brain size and breeding in city centres (likelihood ratio tests: ln brain size: d.f. = 1, χ2 = 11.08, p = 0.0009; ln body size: d.f. = 1, χ2 = 11.26, p = 0.0008). Thus, our results are confirmed by both phylogenetic and non-phylogenetic analyses.

  • 46.
    Maklakov, Alexei A.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Immler, Simone
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Lövlie, Hanne
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Flis, Ilona
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Friberg, Urban
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    The effect of sexual harassment on lethal mutation rate in female Drosophila melanogaster2013In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 280, no 1750, p. 20121874-Article in journal (Refereed)
    Abstract [en]

    The rate by which new mutations are introduced into a population may have far-reaching implications for processes at the population level. Theory assumes that all individuals within a population have the same mutation rate, but this assumption may not be true. Compared with individuals in high condition, those in poor condition may have fewer resources available to invest in DNA repair, resulting in elevated mutation rates. Alternatively, environmentally induced stress can result in increased investment in DNA repair at the expense of reproduction. Here, we directly test whether sexual harassment by males, known to reduce female condition, affects female capacity to alleviate DNA damage in Drosophila melanogaster fruitflies. Female gametes can repair double-strand DNA breaks in sperm, which allows manipulating mutation rate independently from female condition. We show that male harassment strongly not only reduces female fecundity, but also reduces the yield of dominant lethal mutations, supporting the hypothesis that stressed organisms invest relatively more in repair mechanisms. We discuss our results in the light of previous research and suggest that social effects such as density and courtship can play an important and underappreciated role in mediating condition-dependent mutation rate.

  • 47.
    Maklakov, Alexei A.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    Kremer, Natacha
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    Arnqvist, Göran
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Evolution, Animal Ecology.
    The effects of male age at mating on female life-history traits in a seed beetle2007In: Behavioral Ecology, ISSN 1045-2249, E-ISSN 1465-7279, Vol. 18, no 3, p. 551-555Article in journal (Refereed)
    Abstract [en]

    Age at first reproduction is an important component of life history across taxa and can ultimately affect fitness. Because genetic interests of males and females over reproductive decisions commonly differ, theory predicts that conflict may arise over the temporal distribution of matings. To determine the potential for such sexual conflict, we studied the direct costs and benefits associated with mating at different times for females, using seed beetles (Acanthoscelides obtectus) as a model system. Virgin females were resistant to male mating attempts at a very early age but subsequently reduced their resistance. Although we found no difference in life span or mortality rates between females mated early in life and those mated later, females that mated early in life suffered a 12% reduction in lifetime fecundity. Thus, there are direct costs associated with mating early in life for females. Yet, males mate even with newly hatched females. We suggest that these data indicate a potential for sexual conflict over the timing of first mating and that female resistance to mating, at least in part, may represent a female strategy aimed at delaying mating to a later time in life.

  • 48.
    Maklakov, Alexei A.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Lummaa, Virpi
    Evolution of sex differences in lifespan and aging: Causes and constraints2013In: Bioessays, ISSN 0265-9247, E-ISSN 1521-1878, Vol. 35, no 8, p. 717-724Article in journal (Refereed)
    Abstract [en]

    Why do the two sexes have different lifespans and rates of aging? Two hypotheses based on asymmetric inheritance of sex chromosomes (unguarded X) or mitochondrial genomes (mother's curse) explain sex differences in lifespan as sex-specific maladaptation leading to increased mortality in the shorter-lived sex. While asymmetric inheritance hypotheses equate long life with high fitness, considerable empirical evidence suggests that sexes resolve the fundamental tradeoff between reproduction and survival differently resulting in sex-specific optima for lifespan. However, selection for sex-specific values in life-history traits is constrained by intersexual genetic correlations resulting in intra-locus sexual conflict over optimal lifespan. The available data suggest that the evolution of sexual dimorphism only partially resolves these conflicts. Sexual conflict over optimal trait values, which has been demonstrated in model organisms and in humans, is likely to play a key role in shaping the evolution of lifespan, as well as in maintaining genetic variation for sex-specific diseases.

  • 49.
    Maklakov, Alexei A.
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Rowe, Locke
    Friberg, Urban
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Evolutionary Biology.
    Why organisms age: Evolution of senescence under positive pleiotropy?2015In: Bioessays, ISSN 0265-9247, E-ISSN 1521-1878, Vol. 37, no 7, p. 802-807Article in journal (Refereed)
    Abstract [en]

    Two classic theories maintain that aging evolves either because of alleles whose deleterious effects are confined to late life or because of alleles with broad pleiotropic effects that increase early-life fitness at the expense of late-life fitness. However, empirical studies often reveal positive pleiotropy for fitness across age classes, and recent evidence suggests that selection on early-life fitness can decelerate aging and increase lifespan, thereby casting doubt on the current consensus. Here, we briefly review these data and promote the simple argument that aging can evolve under positive pleiotropy between early-and late-life fitness when the deleterious effect of mutations increases with age. We argue that this hypothesis makes testable predictions and is supported by existing evidence.

  • 50.
    Rogell, Björn
    et al.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Widegren, William
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Hallsson, Lára R.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Berger, David
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Björklund, Mats
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Maklakov, Alexei A.
    Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
    Sex-dependent evolution of life-history traits following adaptation to climate warming2014In: Functional Ecology, ISSN 0269-8463, E-ISSN 1365-2435, Vol. 28, no 2, p. 469-478Article in journal (Refereed)
    Abstract [en]

    Summary

    1. Thermodynamic processes increase metabolic rate and decrease longevity at high temperatures in ectotherms. However, how sustained long-term increase in temperature affects the evolution of longevity is poorly understood.
    2. Stress theory of ageing predicts that increased longevity is positively genetically correlated with resistance to different types of environmental stressors implying that evolutionary trajectories of ageing may be mediated by correlative selection for robust phenotypes under thermal stress.
    3. Here, we test this hypothesis by using replicate populations of the seed beetle Callosobruchus maculatus, evolving under two thermal environments: ancestral 30 °C and incremental increase towards novel 36 °C.
    4. Beetles evolving under climate warming became larger, more fecund and lived longer than the beetles evolving under 30 °C across both environments. However, the increase in longevity was partly due to parental effects because after two generations of acclimatization it persisted only in males.
    5. Our results support the hypothesis that evolution of stress resistance confers increased longevity through positive pleiotropy but demonstrate that such effects can be sex specific. These findings suggest that sex differences can evolve as correlated responses to selection under environmental change.
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