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Sex-specific genetic variance for fitness characterized by sex-specific dominance and epistasis
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. (Arnqvist)ORCID iD: 0000-0001-8925-5066
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.ORCID iD: 0000-0002-3501-3376
(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: urn:nbn:se:uu:diva-327275OAI: oai:DiVA.org:uu-327275DiVA, id: diva2:1129979
Funder
EU, European Research Council, GENCON AdG-294333Swedish Research Council, 621-2010-5266Swedish Research Council, 621-2014-4523Available from: 2017-08-08 Created: 2017-08-08 Last updated: 2017-08-11Bibliographically approved
In thesis
1. Sexual conflict, sexual selection, and genetic variance in fitness
Open this publication in new window or tab >>Sexual conflict, sexual selection, and genetic variance in fitness
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:nbn:se:uu:diva-327304 (URN)978-91-513-0022-1 (ISBN)
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

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