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Male-benefit sexually antagonistic genotypes show elevated vulnerability to inbreeding
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.ORCID iD: 0000-0002-3501-3376
2017 (English)In: BMC Evolutionary Biology, ISSN 1471-2148, E-ISSN 1471-2148, Vol. 17, 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.

Place, publisher, year, edition, pages
2017. Vol. 17, 134
Keyword [en]
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: urn:nbn:se:uu:diva-327273DOI: 10.1186/s12862-017-0981-4ISI: 000403408600001PubMedID: 28606137OAI: oai:DiVA.org:uu-327273DiVA: diva2:1129960
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
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. 38 p.
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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