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Sexual selection in males, but not females, purges the standing genetic load in a seed beetle
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.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
(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: urn:nbn:se:uu:diva-327303OAI: oai:DiVA.org:uu-327303DiVA, id: diva2:1130254
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, 2015-05223Available from: 2017-08-08 Created: 2017-08-08 Last updated: 2017-08-08
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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