Asymmetries in courtship signals can result from both developmental instability during ontogeny and from temporary or permanent damage following mating, fighting, or interactions with predators. These two types of asymmetries, which can be divided into fluctuating asymmetry (FA) and damage asymmetry (DA), have both been suggested to play an important role in mate choice as potential honest indicators of phenotypic and/or genetic quality, while at the same time, DA may affect ornament asymmetry in a random manner. Interestingly, despite the massive research effort that has been devoted to the study of asymmetry during the past decades, very little is known about how an individual's behaviour relates to asymmetry. Here, we measure and characterise asymmetry in morphological courtship signals in Corynopoma riisei, a fish where males carry elaborate paddle-like appendices on each side of the body that they display in front of females during courtship. Moreover, we investigate whether male courtship display, employing this bilateral morphological trait, reflects trait asymmetry. Finally, we assess whether males respond to phenotypic manipulations of DA with corresponding changes in courtship behaviour. We show that male display behaviour is asymmetric in a manner that reflects asymmetry of their morphological courtship trait and that male display behaviour responds to manipulations of asymmetry of these paddles. Our results thus suggest that males preferentially use their best side and, hence, that males respond adaptively to temporary changes in signal trait asymmetry.
Recent documentations of sexually antagonistic genetic variation in fitness have spurred an interest in the mechanisms that may act to maintain such variation in natural populations. Using individual-based simulations, I show that positive assortative mating by fitness increases the amount of sexually antagonistic genetic variance in fitness, primarily by elevating the equilibrium frequency of heterozygotes, over most of the range of sex-specific selection and dominance. Further, although the effects of assortative mating by fitness on the protection conditions of polymorphism in sexually antagonistic loci were relatively minor, it widens the protection conditions under most reasonable scenarios (e. g., under heterozygote superiority when fitness is averaged across the sexes) but can also somewhat narrow the protection conditions under other circumstances. The near-ubiquity of assortative mating in nature suggests that it may contribute to upholding standing sexually antagonistic genetic variation in fitness.
Because many journals are currently increasing the rate of pre-peer-review editorial rejects, the editorial criteria upon which such decisions are based are very important. Here, I spotlight 'novelty' as a criterion and argue that it is a very problematic decisive factor at this stage of the editorial process.
Statistics matter greatly in biology, whether we like it or not. As a discipline with an empirical inclination, we are faced with data every day and we rely on inferential statistical models to make sense of it and to provide us with novel insights. Much of the time, the growing level of complexity and sophistication of the models we put to use in ecology and evolution have led to more appropriate analyses of our data. However, this is not always the case. Here, I draw attention to a classic flaw in inferential statistics that has resurfaced in a new flavor as a result of increased reliance on complex linear mixed models -the multifaceted and disturbingly persistent problem of pseudoreplication.
The extent to which mitochondrial DNA (mtDNA) variation is involved in adaptive evolutionary change is currently being reevaluated. In particular, emerging evidence suggests that mtDNA genes coevolve with the nuclear genes with which they interact to form the energy producing enzyme complexes in the mitochondria. This suggests that intergenomic epistasis between mitochondrial and nuclear genes may affect whole-organism metabolic phenotypes. Here, we use crossed combinations of mitochondrial and nuclear lineages of the seed beetle Callosobruchus maculatus and assay metabolic rate under two different temperature regimes. Metabolic rate was affected by an interaction between the mitochondrial and nuclear lineages and the temperature regime. Sequence data suggests that mitochondrial genetic variation has a role in determining the outcome of this interaction. Our genetic dissection of metabolic rate reveals a high level of complexity, encompassing genetic interactions over two genomes, and genotype x genotype x environment interactions. The evolutionary implications of these results are twofold. First, because metabolic rate is at the root of life histories, our results provide insights into the complexity of life-history evolution in general, and thermal adaptation in particular. Second, our results suggest a mechanism that could contribute to the maintenance of nonneutral mtDNA polymorphism.
Our understanding of coevolution between male genitalia and female traits remains incomplete. This is perhaps especially true for genital traits that cause internal injuries in females, such as the spiny genitalia of seed beetles where males with relatively long spines enjoy a high relative fertilization success. We report on a new set of experiments, based on extant selection lines, aimed at assessing the effects of long male spines on females in Callosobruchus maculatus . We first draw on an earlier study using microscale laser surgery, and demonstrate that genital spines have a direct negative (sexually antagonistic) effect on female fecundity. We then ask whether artificial selection for long versus short spines resulted in direct or indirect effects on female lifetime offspring production. Reference females mating with males from long-spine lines had higher offspring production, presumably due to an elevated allocation in males to those ejaculate components that are beneficial to females. Remarkably, selection for long male genital spines also resulted in an evolutionary increase in female offspring production as a correlated response. Our findings thus suggest that female traits that affect their response to male spines are both under direct selection to minimize harm but are also under indirect selection (a good genes effect), consistent with the evolution of mating and fertilization biases being affected by several simultaneous processes.
Wingless female Zeus bugs (genus: Phoreticovelia) produce a secretion from dorsal glands that males feed upon when riding on females. This unique form of sex-role-reversed nuptial feeding may have set the stage for an unusual mating system. Here, we provide natural history details of the mating behaviour for two Zeus bug species. While these species have many mating behaviours in common, the wing morphs within species exhibit entirely different mating strategies. Adult wingless females are ridden permanently by adult wingless males. In the wild, adult sex-ratios among the wingless morph are male-biased; few unmounted adult females exist and many males instead ride immature females who also produce glandular secretions. In contrast, sex-ratios among the winged morph is not male-biased, sexual size dimorphism is less pronounced, females have no dorsal glands and are, consequently, not ridden by males. Field and laboratory observations show that mating is strongly assortative by wing morph. This assortment may allow evolutionary divergence between the two morphs. We discuss the implications of this mating system and suggest that it adds to those studies showing that sexually antagonistic coevolution can be a driver of mating system evolution.
Sensory drive, where the efficacy of a sexual signal depends on the environment in which it is employed, is a potential mechanism behind divergent evolution of secondary sexual traits. Male swordtail characins are equipped with a narrow and transparent extension of the gill cover with a flag-like structure at its tip. This opercular flag mimics a prey item and is employed by males as a 'lure' to attract the attention of females during mating attempts. We conducted a study of genetic and morphological differentiation across swordtail characin populations throughout their native range in Trinidad. The morphology of the opercular flag varied across populations and several aspects of this variation match the predicted hallmarks of sensory drive. First, morphological differentiation of the flag across populations was unrelated to genetic similarity at neutral genetic markers. Second, the shape of the flag covaried with those aspects of body shape that should reflect adaptation to different feeding regimes. Third, and most importantly, the shape of the flag covaried across populations with those environmental characteristics that should most closely reflect differences in local prey abundance. Overall, our results are consistent with a scenario where the evolution of this male sexual signal tracks food-related shifts in female sensory biases across populations, thus providing at least provisional support for a role for sensory drive in population differentiation.
Background: Recent experimental evidence for selection on mitochondrial DNA (mtDNA) has prompted the question as to what processes act to maintain within-population variation in mtDNA. Balancing selection though negative frequency dependent selection (NFDS) among sympatric haplotypes is a possibility, but direct empirical evidence for this is very scarce. Findings: We extend the previous findings of a multi-generation replicated cage experiment in Drosophila subobscura, where mtDNA polymorphism was maintained in a laboratory setting. First, we use a set of Monte Carlo simulations to show that the haplotype frequency dynamics observed are inconsistent with genetic drift alone and most closely match those expected under NFDS. Second, we show that haplotype frequency changes over time were significantly different from those expected under either genetic drift or positive selection but were consistent with those expected under NFSD. Conclusions: Collectively, our analyses provide novel support for NFDS on mtDNA haplotypes, suggesting that mtDNA polymorphism may at least in part be maintained by balancing selection also in natural populations. We very briefly discuss the possible mechanisms that might be involved.
Evolutionary genetics has long struggled with understanding how functional genes under selection remain polymorphic in natural populations. Taking as a starting point that natural selection is ultimately a manifestation of ecological processes, we spotlight an underemphasized and potentially ubiquitous ecological effect that may have fundamental effects on the maintenance of genetic variation. Negative frequency dependency is a well-established emergent property of density dependence in ecology, because the relative profitability of different modes of exploiting or utilizing limiting resources tends to be inversely proportional to their frequency in a population. We suggest that this may often generate negative frequency-dependent selection (NFDS) on major effect loci that affect rate-dependent physiological processes, such as metabolic rate, that are phenotypically manifested as polymorphism in pace-of-life syndromes. When such a locus under NFDS shows stable intermediate frequency polymorphism, this should generate epistatic selection potentially involving large numbers of loci with more minor effects on life-history (LH) traits. When alternative alleles at such loci show sign epistasis with a major effect locus, this associative NFDS will promote the maintenance of polygenic variation in LH genes. We provide examples of the kind of major effect loci that could be involved and suggest empirical avenues that may better inform us on the importance and reach of this process.
Male-female coevolution has taken different paths among closely related species, but our understanding of the factors that govern its direction is limited. While it is clear that ecological factors, life history, and the economics of reproduction are connected, the divergent links are often obscure. We propose that a complete understanding requires the conceptual integration of metabolic phenotypes. Metabolic rate, a nexus of life history evolution, is constrained by ecological factors and may exert important direct and indirect effects on the evolution of sexual dimorphism. We performed standardized experiments in 12 seed beetle species to gain a rich set of sex-specific measures of metabolic phenotypes, life history traits, and the economics of mating and analyzed our multivariate data using phylogenetic comparative methods. Resting metabolic rate (RMR) showed extensive evolution and evolved more rapidly in males than in females. The evolution of RMR was tightly coupled with a suite of life history traits, describing a pace-of-life syndrome (POLS), with indirect effects on the economics of mating. As predicted, high resource competition was associated with a low RMR and a slow POLS. The cost of mating showed sexually antagonistic coevolution, a hallmark of sexual conflict. The sex-specific costs and benefits of mating were predictably related to ecology, primarily through the evolution of male ejaculate size. Overall, our results support the tenet that resource competition affects metabolic processes that, in turn, have predictable effects on both life history evolution and reproduction, such that ecology shows both direct and indirect effects on male-female coevolution.
Efforts to unravel the genomic basis of incipient speciation are hampered by a mismatch between our toolkit and our understanding of the ecology and genetics of adaptation. While the former is focused on detecting selective sweeps involving few independently acting or linked speciation genes, the latter states that divergence typically occurs in polygenic traits under stabilizing selection. Here, we ask whether a role of stabilizing selection on polygenic traits in population divergence may be unveiled by using a phenotypically informed integrative approach, based on genome-wide variation segregating in divergent populations. We compare three divergent populations of seed beetles (Callosobruchus maculatus) where previous work has demonstrated a prominent role for stabilizing selection on, and population divergence in, key life history traits that reflect rate-dependent metabolic processes. We derive and assess predictions regarding the expected pattern of covariation between genetic variation segregating within populations and genetic differentiation between populations. Population differentiation was considerable (mean F-ST = 0.23-0.26) and was primarily built by genes showing high selective constraints and an imbalance in inferred selection in different populations (positive Tajima's D-NS in one and negative in one), and this set of genes was enriched with genes with a metabolic function. Repeatability of relative population differentiation was low at the level of individual genes but higher at the level of broad functional classes, again spotlighting metabolic genes. Absolute differentiation (d(XY)) showed a very different general pattern at this scale of divergence, more consistent with an important role for genetic drift. Although our exploration is consistent with stabilizing selection on polygenic metabolic phenotypes as an important engine of genome-wide relative population divergence and incipient speciation in our study system, we note that it is exceedingly difficult to firmly exclude other scenarios.
The ultimate cause of genome size (GS) evolution in eukaryotes remains a major and unresolved puzzle in evolutionary biology. Large-scale comparative studies have failed to find consistent correlations between GS and organismal properties, resulting in the 'C-value paradox'. Current hypotheses for the evolution of GS are based either on the balance between mutational events and drift or on natural selection acting upon standing genetic variation in GS. It is, however, currently very difficult to evaluate the role of selection because within-species studies that relate variation in life-history traits to variation in GS are very rare. Here, we report phylogenetic comparative analyses of GS evolution in seed beetles at two distinct taxonomic scales, which combines replicated estimation of GS with experimental assays of life-history traits and reproductive fitness. GS showed rapid and bidirectional evolution across species, but did not show correlated evolution with any of several indices of the relative importance of genetic drift. Within a single species, GS varied by 4-5% across populations and showed positive correlated evolution with independent estimates of male and female reproductive fitness. Collectively, the phylogenetic pattern of GS diversification across and within species in conjunction with the pattern of correlated evolution between GS and fitness provide novel support for the tenet that natural selection plays a key role in shaping GS evolution.
Although males and females share much of the same genome, selection is often distinct in the two sexes. Sexually antagonistic loci will in theory cause a gender load in populations, because sex-specific selection on a given trait in one sex will compromise the adaptive evolution of the same trait in the other sex. However, it is currently not clear whether such intralocus sexual conflict (ISC) represents a transient evolutionary state, where conflict is rapidly resolved by the evolution of sexual dimorphism (SD), or whether it is a more chronic impediment to adaptation. All else being equal, ISC should manifest itself as correlated evolution between population fitness and SD in traits expressed in both sexes. However, comparative tests of this prediction are problematic and have been unfeasible. Here, we assess the effects of ISC by comparing fitness and SD across distinct laboratory populations of seed beetles that should be well adapted to a shared environment. We show that SD in juvenile development time, a key life-history trait with a history of sexually antagonistic selection in this model system, is positively related to fitness. This effect is due to a correlated evolution between population fitness and development time that is positive in females but negative in males. Loosening the genetic bind between the sexes has evidently allowed the sexes to approach their distinct adaptive peaks.
There is increasing evidence of segregating sexually antagonistic (SA) genetic variation for fitness in laboratory and wild populations, yet the conditions for the maintenance of such variation can be restrictive. Epistatic interactions between genes can contribute to the maintenance of genetic variance in fitness and we suggest that epistasis between SA genes should be pervasive. Here, we explore its effect on SA genetic variation in fitness using a two locus model with negative epistasis. Our results demonstrate that epistasis often increases the parameter space showing polymorphism for SA loci. This is because selection in one locus is affected by allele frequencies at the other, which can act to balance net selection in males and females. Increased linkage between SA loci had more marginal effects. We also show that under some conditions, large portions of the parameter space evolve to a state where male benefit alleles are fixed at one locus and female benefit alleles at the other. This novel effect of epistasis on SA loci, which we term the 'equity effect', may have important effects on population differentiation and may contribute to speciation. More generally, these results support the suggestion that epistasis contributes to population divergence.
BACKGROUND: Sexual dimorphism in immunity is believed to reflect sex differences in reproductive strategies and trade-offs between competing life history demands. Sexual selection can have major effects on mating rates and sex-specific costs of mating and may thereby influence sex differences in immunity as well as associated host-pathogen dynamics. Yet, experimental evidence linking the mating system to evolved sexual dimorphism in immunity are scarce and the direct effects of mating rate on immunity are not well established. Here, we use transcriptomic analyses, experimental evolution and phylogenetic comparative methods to study the association between the mating system and sexual dimorphism in immunity in seed beetles, where mating causes internal injuries in females.
RESULTS: We demonstrate that female phenoloxidase (PO) activity, involved in wound healing and defence against parasitic infections, is elevated relative to males. This difference is accompanied by concomitant sex differences in the expression of genes in the prophenoloxidase activating cascade. We document substantial phenotypic plasticity in female PO activity in response to mating and show that experimental evolution under enforced monogamy (resulting in low remating rates and reduced sexual conflict relative to natural polygamy) rapidly decreases female (but not male) PO activity. Moreover, monogamous females had evolved increased tolerance to bacterial infection unrelated to mating, implying that female responses to costly mating may trade off with other aspects of immune defence, an hypothesis which broadly accords with the documented sex differences in gene expression. Finally, female (but not male) PO activity shows correlated evolution with the perceived harmfulness of male genitalia across 12 species of seed beetles, suggesting that sexual conflict has a significant influence on sexual dimorphisms in immunity in this group of insects.
CONCLUSIONS: Our study provides insights into the links between sexual conflict and sexual dimorphism in immunity and suggests that selection pressures moulded by mating interactions can lead to a sex-specific mosaic of immune responses with important implications for host-pathogen dynamics in sexually reproducing organisms.
The seed beetle Callosobruchus maculatus is a significant agricultural pest and increasingly studied model of sexual conflict. Males possess genital spines that increase the transfer of seminal fluid proteins (SFPs) into the female body. As SFPs alter female behaviour and physiology, they are likely to modulate reproduction and sexual conflict in this species. Here, we identified SFPs using proteomics combined with a de novo transcriptome. A prior 2D-sodium dodecyl sulphate polyacrylamide gel electrophoresis analysis identified male accessory gland protein spots that were probably transferred to the female at mating. Proteomic analysis of these spots identified 98 proteins, a majority of which were also present within ejaculates collected from females. Standard annotation workflows revealed common functional groups for SFPs, including proteases and metabolic proteins. Transcriptomic analysis found 84 transcripts differentially expressed between the sexes. Notably, genes encoding 15 proteins were highly expressed in male abdomens and only negligibly expressed within females. Most of these sequences corresponded to 'unknown' proteins (nine of 15) and may represent rapidly evolving SFPs novel to seed beetles. Our combined analyses highlight 44 proteins for which there is strong evidence that they are SFPs. These results can inform further investigation, to better understand the molecular mechanisms of sexual conflict in seed beetles.
The male ejaculate contains a multitude of seminal fluid proteins (SFPs), many of which are key reproductive molecules, as well as sperm. However, the identification of SFPs is notoriously difficult and a detailed understanding of this complex phenotype has only been achieved in a few model species. We employed a recently developed proteomic method involving whole-organism stable isotope labelling coupled with proteomic and transcriptomic analyses to characterize ejaculate proteins in the seed beetle Callosobruchus maculatus. We identified 317 proteins that were transferred to females at mating, and a great majority of these showed signals of secretion and were highly male-biased in expression in the abdomen. These male-derived proteins were enriched with proteins involved in general metabolic and catabolic processes but also with proteolytic enzymes and proteins involved in protection against oxidative stress. Thirty-seven proteins showed significant homology with SFPs previously identified in other insects. However, no less than 92 C. maculatus ejaculate proteins were entirely novel, receiving no significant blast hits and lacking homologs in extant data bases, consistent with a rapid and divergent evolution of SFPs. We used 3D micro-tomography in conjunction with proteomic methods to identify 5 distinct pairs of male accessory reproductive glands and to show that certain ejaculate proteins were only recovered in certain male glands. Finally, we provide a tentative list of 231 candidate female-derived reproductive proteins, some of which are likely important in ejaculate processing and/or sperm storage.
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.
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.
Mutation has a fundamental influence over evolutionary processes, but how evolutionary processes shape mutation rate remains less clear. In asexual unicellular organism, increased mutation rates have been observed in stressful environments and the reigning paradigm ascribes this increase to selection for evolvability. However, this explanation does not apply in sexually reproducing species, where little is known about how the environment affects mutation rate. Here we challenged experimental lines of seed beetle, evolved at ancestral temperature or under simulated climate warming, to repair induced mutations at ancestral and stressful temperature. Results show that temperature stress causes individuals to pass on a greater mutation load to their grand-offspring. This suggests that stress-induced mutation rates, in unicellular and multicellular organisms alike, can result from compromised germline DNA repair in low condition individuals. Moreover, lines adapted to simulated climate warming had evolved increased longevity at the cost of reproduction, and this allocation decision improved germline repair. These results suggest that mutation rates can be modulated by resource allocation trade-offs encompassing life-history traits and the germline and have important implications for rates of adaptation and extinction as well as our understanding of genetic diversity in multicellular organisms.
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.
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.
Despite the costs of mating, females of most taxa mate with multiple males. Polyandrous females are hypothesized to gain genetic benefits for their offspring, but this assumes paternity bias favoring male genotypes that enhance offspring viability. We determined net male genetic effects on female and offspring fitness in a seed beetle and then tested whether fertilization success was biased in favor of high-quality male genotypes in double mating experiments. Contrary to expectations, high-quality male genotypes consistently had a lower postmating fertilization success in two independent assays. Our results imply that sexually antagonistic adaptations have a major and unappreciated influence on male postmating fertilization success. Such genetic variation renders indirect genetic benefits an unlikely driver of the evolution of polyandry.
Our general understanding of the evolution of genome size (GS) is incomplete, and it has long been clear that GS does not reflect organismal complexity. Here, we assess the hypothesis that larger genomes may allow organisms to better cope with environmental variation. It is, for example, possible that genome expansion due to proliferation of transposable elements or gene duplications may affect the ability to regulate and fine-tune transcriptional profiles. We used 18 populations of the seed beetle Callosobruchus maculatus, which differ in GS by up to 4.5%, and exposed adults and juveniles to environmental stress in a series of experiments where stage-specific fitness was assayed. We found that populations with larger genomes were indeed better buffered against environmental stress for adult, but not for juvenile, fitness. The genetic correlation across populations between GS and canalization of adult fitness is consistent with a role for natural selection in the evolution of GS.
Sexual selection imposed by mating preferences is often implicated in the evolution of both sexual dimorphism and divergence between species in signalling traits. Epicuticular compounds (ECs) are important signalling traits in insects and show extensive variability among and within taxa. Here, we investigate whether variation in the multivariate EC profiles of two sex role-reversed beetle species, Megabruchidius dorsalis and Megabruchidius tonkineus, predicts mate attractiveness and mating success in males and females. The two species had highly distinct EC profiles and both showed significant sexual dimorphism in ECs. Age and mating status in both species were also distinguishable by EC profile. Males and females of both species showed significant association between their EC profile and attractiveness, measured both as latency to mating and as success in mate-choice trials. Remarkably, the major multivariate vector describing attractiveness was correlated in both species, both sexes, and in both choice and no-choice experiments such that increased attractiveness was in all cases associated with a similar multivariate modification of EC composition. Furthermore, in both sexes this vector of attractiveness was associated with more male-like EC profiles, as well as those characterizing younger and nonvirgin individuals, which might reflect a general preference for individuals of high condition in both sexes. Despite significant sexual selection on EC composition, however, we found no support for the proposition that sexual selection is responsible for divergence in ECs between these species.
When males provide females with resources at mating, they can become the limiting sex in reproduction, in extreme cases leading to the reversal of typical courtship roles. The evolution of male provisioning is thought to be driven by male reproductive competition and selection for female fecundity enhancement. We used experimental evolution under male- or female-biased sex ratios and limited or unlimited food regimes to investigate the relative roles of these routes to male provisioning in a sex role-reversed beetle, Megabruchidius tonkineus, where males provide females with nutritious ejaculates. Males evolving under male-biased sex ratios transferred larger ejaculates than did males from female-biased populations, demonstrating a sizeable role for reproductive competition in the evolution of male provisioning. Although larger ejaculates elevated female lifetime offspring production, we found little evidence of selection for larger ejaculates via fecundity enhancement: males evolving under resource-limited and unlimited conditions did not differ in mean ejaculate size. Resource limitation did, however, affect the evolution of conditional ejaculate allocation. Our results suggest that the resource provisioning that underpins sex role reversal in this system is the result of male-male reproductive competition rather than of direct selection for males to enhance female fecundity.
The role of mitochondrial DNA for the evolution of life-history traits remains debated. We examined mitonuclear effects on the activity of the multisubunit complex of the electron transport chain (ETC) involved in oxidative phosphorylation (OXPHOS) across lines of the seed beetle Acanthoscelides obtectus selected for a short (E) or a long (L) life for more than >160 generations. We constructed and phenotyped mitonuclear introgression lines, which allowed us to assess the independent effects of the evolutionary history of the nuclear and the mitochondrial genome. The nuclear genome was responsible for the largest share of divergence seen in ageing. However, the mitochondrial genome also had sizeable effects, which were sex-specific and expressed primarily as epistatic interactions with the nuclear genome. The effects of mitonuclear disruption were largely consistent with mitonuclear coadaptation. Variation in ETC activity explained a large proportion of variance in ageing and life-history traits and this multivariate relationship differed somewhat between the sexes. In conclusion, mitonuclear epistasis has played an important role in the laboratory evolution of ETC complex activity, ageing, and life histories and these are closely associated. The mitonuclear architecture of evolved differences in life-history traits and mitochondrial bioenergetics was sex-specific.
Traumatic mating (or copulatory wounding) is an extreme form of sexual conflict whereby male genitalia physically harm females during mating. In such species females are expected to evolve counter-adaptations to reduce male-induced harm. Importantly, female counter-adaptations may include both genital and non-genital traits. in this study, we examine evolutionary associations between harmful male genital morphology and female reproductive tract morphology and immune function across 13 populations of the seed beetle Callosobruchus maculatus. We detected positive correlated evolution between the injuriousness of male genitalia and putative female resistance adaptations across populations. Moreover, we found evidence for a negative relationship between female immunity and population productivity, which suggests that investment in female resistance may be costly due to the resource trade-offs that are predicted between immunity and reproduction. Finally, the degree of female tract scarring (harm to females) was greater in those populations with both longer aedeagal spines and a thinner female tract lining. Our results are thus consistent with a sexual arms race, which is only apparent when both male and female traits are taken into account. Importantly, our study provides rare evidence for sexually antagonistic coevolution of male and female traits at the within-species level.
The integration of the mitochondrial and nuclear genomes coordinates cellular energy production and is fundamental to life among eukaryotes. Therefore, there is potential for strong selection to shape the interactions between the two genomes. Several studies have now demonstrated that epistatic interactions between cytoplasmic and nuclear genes for fitness can occur both at a "within" and "across" population level. Genotype-by-environment interactions are common for traits that are encoded by nuclear genes, but the effects of environmental heterogeneity on traits that are partly encoded by cytoplasmic genes have received little attention despite the fact that there are reasons to believe that phenotypic effects of cytoplasmic genetic variation may often be environment specific. Consequently, the importance of environmental heterogeneity to the outcomes of cyto-nuclear fitness interactions and to the maintenance of mitochondrial polymorphism is unclear. Here, we assess the influence of temperature on cyto-nuclear effects on egg-to-adult development time in seed beetles (Callosobruchus maculatus). We employed an "across-population" design, sourcing beetles from five distinct populations and using backcrossing to create orthogonal combinations of distinct introgression lines, fixed for their cytoplasmic and nuclear lineages. We then assayed development times at two different temperatures and found sizeable cyto-nuclear effects in general, as well as temperature- and block-specific cyto-nuclear effects. These results demonstrate that environmental factors such as temperature do exert selection on cytoplasmic genes by favoring specific cyto-nuclear genetic combinations, and are consistent with the suggestion that complex genotype-by-environment interactions may promote the maintenance of polymorphism in mitochondrial genes.
It is widely assumed that male sperm competitiveness evolves adaptively. However, recent studies have found a cytoplasmic genetic component to phenotypic variation in some sperm traits presumed important in sperm competition. As cytoplasmic genes are maternally transmitted, they cannot respond to selection on sperm and this constraint may affect the scope in which sperm competitiveness can evolve adaptively. We examined nuclear and cytoplasmic genetic contributions to sperm competitiveness, using populations of Callosobruchus maculatus carrying orthogonal combinations of nuclear and cytoplasmic lineages. Our design also enabled us to examine genetic contributions to female remating. We found that sperm competitiveness and remating are primarily encoded by nuclear genes. In particular, a male's sperm competitiveness phenotype was contingent on an interaction between the competing male genotypes. Furthermore, cytoplasmic effects were detected on remating but not sperm competitiveness, suggesting that cytoplasmic genes do not generally play a profound evolutionary role in sperm competition.
The symbiotic relationship between the mitochondrial and nuclear genomes coordinates metabolic energy production and is fundamental to life among eukaryotes. Consequently, there is potential for strong selection to shape interactions between these two genomes. Substantial research attention has focused on the possibility that within-population sequence polymorphism in mitochondrial DNA (mtDNA) is maintained by mitonuclear fitness interactions. Early theory predicted that selection will often eliminate mitochondrial polymorphisms. However, recent models demonstrate that intergenomic interactions can promote the maintenance of polymorphism, especially if the nuclear genes involved are linked to the X chromosome. Most empirical studies to date that have assessed cytonuclear fitness interactions have studied variation across populations and it is still unclear how general and strong such interactions are within populations. We experimentally tested for cytonuclear interactions within a laboratory population of Drosophila melanogaster using 25 randomly sampled cytoplasmic genomes, expressed in three different haploid nuclear genetic backgrounds, while eliminating confounding effects of intracellular bacteria (e.g., Wolbachia). We found sizable cytonuclear fitness interactions within this population and present limited evidence suggesting that these effects were sex specific. Moreover, the relative fitness of cytonuclear genotypes was environment specific. Sequencing of mtDNA (2752 bp) revealed polymorphism within the population, suggesting that the observed cytoplasmic genetic effects may be mitochondrial in origin.
Sperm competition theory predicts that sperm traits influencing male fertilizing ability will evolve adaptively. However, it has been suggested that some sperm traits may be at least partly encoded by mitochondrial genes. If true, this may constrain the adaptive evolution of such traits because mitochondrial DNA (mtDNA) is maternally inherited and there is thus no selection on mtDNA in males. Phenotypic variation in such traits may nevertheless be high because mutations in mtDNA that have deleterious effects on male traits, but neutral or beneficial effects in females, may be maintained by random processes or selection in females. We used backcrossing to create introgression lines of seed beetles (Callosobruchus maculatus), carrying orthogonal combinations of distinct lineages of cytoplasmic and nuclear genes, and then assayed sperm viability and sperm length in all lines. We found sizeable cytoplasmic effects on both sperm traits and our analyses also suggested that the cytoplasmic effects varied across nuclear genetic backgrounds. We discuss some potential implications of these findings for sperm competition theory.
Recent studies have uncovered an abundance of non-neutral cytoplasmic genetic variation within species, which suggests that we should no longer consider the cytoplasm an idle intermediary of evolutionary change. Nonneutrality of cytoplasmic genomes is particularly intriguing, given that these genomes are maternally transmitted. This means that the fate of any given cytoplasmic genetic mutation is directly tied to its performance when expressed in females. For this reason, it has been hypothesized that cytoplasmic genes will coevolve via a sexually antagonistic arms race with the biparentally transmitted nuclear genes with which they interact. We assess this prediction, examining the intergenomic contributions to the costs and benefits of mating in Callosobruchus maculatus females subjected to a mating treatment with three classes (kept virgin, mated once, or forced to cohabit with a male). We find no evidence that the economics of mating are determined by interactions between cytoplasmic genes expressed in females and nuclear genes expressed in males and, therefore, no support for a sexually antagonistic intergenomic arms race. The cost of mating to females was, however, shaped by an interaction between the cytoplasmic and nuclear genes expressed within females. Thus, cytonuclear interactions are embroiled in the economics of mating.
Whether females gain indirect genetic benefits through mate choice is a controversial issue since this requires additive genetic variance in the preferred male traits. Condition dependence could maintain the necessary genetic variance by linking the expression of male traits to the supposedly large number of genes affecting condition. Copulating males of the red flour beetle Tribolium castaneum rub their legs along the female elytra. Females favor males with vigorous rubbing through cryptic female choice. We measured the repeatability and heritability of this behavior and assessed its potential use as indicator of viability and condition. We found genetic variance in larval to adult survival and in the rate of leg rubbing in males. However, the rate of leg rubbing was not related to offspring survival or condition dependent. The genetic variance in leg rubbing was mostly non-additive with very low narrow sense heritability. Therefore, we failed to document any indirect genetic benefits to choosy females through viability of their offspring or attractiveness of their sons.
Mate attractiveness is known to sometimes influence female reproductive investment (i.e. differential allocation) and the sex ratio of her offspring (i.e. sex allocation). Males of the red flour beetle Tribolium castaneum rub the lateral edges of the females’ elytra with their tarsi during copulation. This behavior is important for paternity success when females have mated with two males. We manipulated female perception of the leg rubbing behavior by tarsal ablation and tested whether this behavior is also favored through differential allocation and whether it affects sex allocation. We found some support for an increase in female oviposition rate in response to intensive leg rubbing but failed to find any support for an effect on sex allocation. The overall sex ratio of offspring was slightly male biased but females did not appear to regulate the sex ratio of their offspring.