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Sexual conflict, sexual selection, and genetic variance in fitness
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. (Arnqvist)ORCID iD: 0000-0001-8925-5066
2017 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Understanding sex-specific genetic variance for fitness is of fundamental importance to our understanding of evolution. This thesis presents the findings of empirical investigations into sex-specific genetic variance in fitness. The findings are discussed in terms of their implications for our understanding of the classic evolutionary paradoxes of what maintains genetic variance in fitness and what maintains sexual reproduction, as well as more specific implications regarding adaptation and population viability. Males and females reproduce and accrue fitness in fundamentally different ways, which inevitably comes at a detriment to the fitness of individuals of the opposite sex. This is known as sexual conflict, and because males and females use largely the same genome to develop, grow and reproduce, a genetic tug-of-war ensues. Alternative alleles at sexually antagonistic (SA) genes have opposing fitness effects in males and females. The consequence of this genetic tug-of-war is that alternative allelic variants at SA loci can be maintained in the population. Such SA genetic variation can therefore maintain genetic variance for fitness. Variance in fitness can also be maintained by a constant influx of mutations with weakly deleterious effects and weak selection against them, in what is referred to as mutation-selection balance. Because the average deleterious mutation will be detrimental to both sexes, this source of genetic variance in fitness will have predominantly sexually concordant (SC) effects. This thesis uses a wild-caught population of the seed beetle Callosobruchus maculatus to investigate these two mechanisms of maintaining genetic variance in fitness, as well as the consequences they bear on adaptation, population viability, and the maintenance of sexual reproduction. Results largely support much of the theoretical expectations for sexual conflict, sexual selection and maintenance of genetic variance in fitness, as well as stimulate new thoughts and hypotheses about the nature of SA genetic variation and its interaction with weakly deleterious partially recessive mutations.

Abstract [sv]

Vår kunskap om könsspecifik selektion och genetisk variation för fitness är central för förståelsen av evolutionära processer. I den här avhandligen presenteras resultaten av empiriska undersökningar av just könsspecifik genetisk variation för fitness. Resultaten diskuteras med fokus på deras betydelse för de klassiska evolutionära paradoxerna angående vad som bibehåller genetisk variation i fitness och varför organismer som förökar sig sexuellt är så vanliga, men även mer specifika konsekvenser för en populations anpassningsförmåga och livskraftighet avhandlas. Evolutionen har ofta gynnat olika reproduktiva strategier hos hannar och honor, och dessa strategier kan medföra kostnader för det motsatta könet. Den könskonflikt som uppstår på grund av detta kan också inbegripa en genetisk dragkamp eftersom könen delar genetisk arvsmassa men gynnas av olika anpassningar. Konsekvensen är att alternativa varianter av gener gynnas hos honor och hanar, vilket resulterar i en form av balanserande selektion som kan bibehålla genetisk variation i en population. Genetisk variation i fitness kan även upprätthållas genom en jämvikt mellan ett konstant inflöde av genetisk variation via mutationer med svagt negativ effekt och svag selektion mot dessa mutationer.  Eftersom en negativ mutation normalt kommer vara skadlig för båda könen kommer den här typen av källa till genetisk variation i fitness ha liknande effekt hos könen.  I arbetet med denna avhandlig har jag använt en vilt infångad population av fröbaggaen Callosobruchus maculatus för att undersöka dessa två underliggande mekanismer bakom upprätthållandet av genetisk variation för fitness, samt vilka potentiella konsekvenser de kan ha för en populations anpassningsförmåga och för bibehållandet av sexuell reproduktion. Resultaten i denna avhandling stödjer i stort många av de antaganden som ligger till grund för teorin om könskonflikter, sexuell selektion och vad som upprätthåller genetisk variation för fitness. Resultaten ger också upphov till nya idéer och hypoteser angående  genetisk variation med könsspecifika effekter och dess interaktion med partiellt recessiva negativa mutationer.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2017. , p. 38
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1538
National Category
Natural Sciences
Research subject
Biology with specialization in Animal Ecology
Identifiers
URN: urn:nbn:se:uu:diva-327304ISBN: 978-91-513-0022-1 (print)OAI: oai:DiVA.org:uu-327304DiVA, id: diva2:1130259
Public defence
2017-09-22, Zootissalen, Norbyv. 18, Uppsala, 10:00 (English)
Opponent
Supervisors
Funder
EU, European Research Council, GENCON AdG-294333Swedish Research Council, 621-2010-5266Swedish Research Council, 621-2014-4523Swedish Research Council, 2015-05223
Note

The alternative abstract I uploaded should be used as the Swedish summary.

Available from: 2017-08-25 Created: 2017-08-08 Last updated: 2017-09-08
List of papers
1. Intralocus Sexual Conflict and Environmental Stress
Open this publication in new window or tab >>Intralocus Sexual Conflict and Environmental Stress
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2014 (English)In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 68, no 8, p. 2184-2196Article in journal (Refereed) Published
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.

Keyword
Adaptation, condition dependence, genetic quality, sexual selection, sexually antagonistic, temperature
National Category
Ecology Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-232012 (URN)10.1111/evo.12439 (DOI)000340470600003 ()
Funder
Swedish Research Council, 621-2010-5266EU, European Research Council, AdG-294333
Available from: 2014-09-15 Created: 2014-09-12 Last updated: 2017-12-05Bibliographically approved
2. Strong sexual selection in males against a mutation load that reduces offspring production in seed beetles
Open this publication in new window or tab >>Strong sexual selection in males against a mutation load that reduces offspring production in seed beetles
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2016 (English)In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 29, no 6, p. 1201-1210Article in journal (Refereed) Published
Abstract [en]

Theory predicts that sexual reproduction can increase population viability relative to asexual reproduction by allowing sexual selection in males to remove deleterious mutations from the population without large demographic costs. This requires that selection acts more strongly in males than females and that mutations affecting male reproductive success have pleiotropic effects on population productivity, but empirical support for these assumptions is mixed. We used the seed beetle Callosobruchus maculatus to implement a three-generation breeding design where we induced mutations via ionizing radiation (IR) in the F-0 generation and measured mutational effects (relative to nonirradiated controls) on an estimate of population productivity in the F-1 and effects on sex-specific competitive lifetime reproductive success (LRS) in the F-2. Regardless of whether mutations were induced via F-0 males or females, they had strong negative effects on male LRS, but a nonsignificant influence on female LRS, suggesting that selection is more efficient in removing deleterious alleles in males. Moreover, mutations had seemingly shared effects on population productivity and competitive LRS in both sexes. Thus, our results lend support to the hypothesis that strong sexual selection on males can act to remove the mutation load on population viability, thereby offering a benefit to sexual reproduction.

Keyword
adaptation, genetic correlation, intralocus sexual conflict, pleiotropy, population viability, sexual antagonism, sexual selection
National Category
Biological Sciences
Identifiers
urn:nbn:se:uu:diva-304536 (URN)10.1111/jeb.12862 (DOI)000382498900009 ()26991346 (PubMedID)
Funder
EU, European Research Council, AdG-294333Swedish Research Council, 621-2010-5266
Available from: 2016-10-12 Created: 2016-10-06 Last updated: 2017-08-08Bibliographically approved
3. Male-benefit sexually antagonistic genotypes show elevated vulnerability to inbreeding
Open this publication in new window or tab >>Male-benefit sexually antagonistic genotypes show elevated vulnerability to inbreeding
2017 (English)In: BMC Evolutionary Biology, ISSN 1471-2148, E-ISSN 1471-2148, Vol. 17, article id 134Article in journal (Refereed) Published
Abstract [en]

Background

There is theoretical and empirical evidence for strong sexual selection in males having positive effects on population viability by serving to purify the genome of its mutation load at a low demographic cost. However, there is also theoretical and empirical evidence for negative effects of sexual selection on female fitness, and therefore population viability, known as the gender load. This can take the form of sexually antagonistic (SA) genetic variation where alleles with a selective advantage in males pose a detriment to female fitness, and vice versa. Here, using seed beetles, we shed light on a previously unexplored manifestation of the gender load: the effect of SA genetic variation on tolerance to inbreeding.

Results

We found that genotypes encoding high male, but low female fitness exhibited significantly greater rates of extinction upon enforced inbreeding relative to genotypes encoding high female but low male fitness. Also, genotypes encoding low fitness in both sexes exhibited greater rates of extinction relative to generally high-fitness genotypes (though marginally non-significant), an expected finding attributable to variation in mutation load across genotypes. Despite follow-up investigations aiming to identify the mechanism(s) underlying these findings, it remains unclear whether the gender load and the mutation load have independent consequences for tolerance to inbreeding, or whether these two types of genetic architecture interact epistatically to render male-benefit genetic variation relatively intolerant to inbreeding.

Conclusions

Regardless of the underlying mechanism(s), our results show that male-benefit/female-detriment SA genetic variation poses a previously unseen detriment to population viability due to its elevated vulnerability to inbreeding/homozygosity. This suggests that sexual selection in the context of SA genetic variance for fitness may enhance the gender load on population viability more than previously appreciated, due to selecting for male-benefit SA genetic variation that engenders lineages to extinction upon inbreeding. We note that our results imply that SA alleles that are sexually selected for in males may be underrepresented or even lacking in panels of inbred lines.

Keyword
Antagonistic pleiotropy, Balancing selection, Fitness, Genetic variation, Inbreeding depression, Intralocus sexual conflict, Mutation load, Sexually antagonistic selection
National Category
Evolutionary Biology
Research subject
Biology with specialization in Animal Ecology
Identifiers
urn:nbn:se:uu:diva-327273 (URN)10.1186/s12862-017-0981-4 (DOI)000403408600001 ()28606137 (PubMedID)
Funder
EU, European Research Council, GENCON AdG-294333Swedish Research Council, 621-2010-5266Swedish Research Council, 621-2014-4523
Available from: 2017-08-08 Created: 2017-08-08 Last updated: 2017-11-29Bibliographically approved
4. Sex-specific genetic variance for fitness characterized by sex-specific dominance and epistasis
Open this publication in new window or tab >>Sex-specific genetic variance for fitness characterized by sex-specific dominance and epistasis
(English)Manuscript (preprint) (Other academic)
Abstract [en]

The ubiquity of sexually antagonistic (SA) genetic variation for fitness suggests that antagonistic pleiotropy is one of the most likely and widespread mechanisms of balancing selection acting to maintain genetic variance for fitness. However, stable polymorphism via antagonistic pleiotropy requires dominance reversal for fitness—sex-specific dominance in the context of SA pleiotropy. Despite this possibly crucial role for sex-specific dominance reversal in maintaining genetic variance for fitness, it has rarely been addressed empirically. In addition to dominance reversal, SA epistasis, sex-biased gene expression (SBGE), and parental effects may also aid the maintenance genetic polymorphisms for fitness under SA selection. Here, we performed a full diallel cross among 16 inbred strains of a population of the seed beetle Callosobruchus maculatus. We measured sex-specific competitive lifetime reproductive success (i.e. fitness) in the F1, for a total of 3278 individual fitness assays over 512 possible genetic combinations. Using Bayesian and restricted maximum likelihood (REML) diallel analyses in parallel, we partitioned phenotypic variance for fitness (after accounting for the effect of inbreeding) into additive genetic variance, parental effects, dominance, epistasis, asymmetric epistasis, and sex-specific versions thereof. Sex-specific variance in fitness exhibited pronounced contributions from dominance, sex-specific dominance, epistasis, and sex-specific epistasis, supporting a role for sex-specific dominance reversal and SA epistasis in contributing to the maintenance of SA genetic variance for fitness. To our knowledge, this is the first detailed diallel partitioning of the sex-specific genetic architecture for fitness, shedding new light on an old question.

National Category
Natural Sciences
Research subject
Biology with specialization in Animal Ecology
Identifiers
urn:nbn:se:uu:diva-327275 (URN)
Funder
EU, European Research Council, GENCON AdG-294333Swedish Research Council, 621-2010-5266Swedish Research Council, 621-2014-4523
Available from: 2017-08-08 Created: 2017-08-08 Last updated: 2017-08-11Bibliographically approved
5. Sexual selection in males, but not females, purges the standing genetic load in a seed beetle
Open this publication in new window or tab >>Sexual selection in males, but not females, purges the standing genetic load in a seed beetle
(English)Manuscript (preprint) (Other academic)
Abstract [en]

The concept of genic capture revealing the genetic quality in males is central to sexual selection theory and the potential for males to purge a population’s weakly deleterious partially recessive mutation load. However, empirical demonstrations of sexual selection in males purging the standing genetic load on a population are almost completely lacking, perhaps in part because of the partially hidden/recessive nature of mutation load limiting its detection. Here, we exposed mutation load by experimentally increasing homozygosity in 16 strains of the seed beetle Callosobruchus maculatus isolated from a natural population. We then assessed the potential for selection to purge load in males and females separately by correlating the breeding values for variance in competitive lifetime reproductive success (i.e. fitness) among the outbred combinations of those strains with the difference between outbred and inbred breeding values for fitness (i.e. mutation load), in a way that avoided correlating confounded variables. Outbred breeding values for male fitness were significantly negatively correlated with mutation load, demonstrating the ability of males to purge mutation load. Breeding values for female fitness, however, were uncorrelated to mutation load, likely because female fitness did not vary enough to reflect genetic quality. Thus, our results are consistent with an additional value to sexual reproduction beyond recombination: whereas females experience relatively weak selection, limiting purging of their own mutation load, this may be achieved by producing males and having them compete intensely for access to their eggs, such that only those of high genetic quality contribute to the next generation. These results have important implications for our understanding of sexual selection, the maintenance of variation in fitness-related traits, and the prevalence of sexual reproduction.

National Category
Natural Sciences
Research subject
Biology with specialization in Animal Ecology
Identifiers
urn:nbn:se:uu:diva-327303 (URN)
Projects
Karl Grieshop_Doctoral thesis
Funder
EU, European Research Council, GENCON AdG-294333Swedish Research Council, 621-2010-5266Swedish Research Council, 621-2014-4523Swedish Research Council, 2015-05223
Available from: 2017-08-08 Created: 2017-08-08 Last updated: 2017-08-08

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