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Sexual Selection and Adaptation to Novel Environments
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.
2017 (English)Doctoral thesis, comprehensive summary (Other academic)
Description
Abstract [en]

The work included in this thesis aims at exploring the environmental sensitivity of benefits and costs of sexual selection through a combined empirical and theoretical effort, to increase our understanding of the impact of environmental change on sexually reproducing populations.Can sexual selection promote adaptation to novel environments? Sexual selection for good genes should accelerate adaptation by granting higher reproductive success to individuals of high genetic quality. However, sexual conflict is a frequent outcome of sexual reproduction and may often be detrimental to population fitness. Experimental evolution has shown that the role of sexual selection in adaptation is variable, because of a complex balance between the detrimental and beneficial effects described above.The present thesis is investigating the role of sexual selection in adaptation by focusing on the sex-specific strength of selection and the intensity of intralocus sexual conflict (IaSC) in ancestral and novel environments. The sex-specific strength of selection is a valuable proxy for the benefits of sexual reproduction, since a male-bias in selection caused by sexual selection should allow efficient purging of deleterious alleles with little impact on female fecundity and cost to population fitness.This thesis investigates both sex-specific selection and IaSC across benign and novel environments in two species of seed beetles, Callosobruchus maculatus and Acanthoscelides obtectus, and includes a theoretical model of the effect of environmental change on of sexual selection. The empirical part of my results indicates that, generally, selection at the adult stage is male biased but that this male bias may be reduced under stress, pointing towards reduced benefits of sexual selection under rapid environmental change. Additional simulations suggest that the frequency dependent nature of sexual selection alone could explain this trend. No empirical support was found for the reduction of IaSC under stress.It is becoming crucial today to understand the impact of environmental change on natural populations. This thesis brings new material adding to our understanding of the role of sexual selection within that particular issue. The outcome of sexual selection is dependent on a variety of mechanisms, such as good genes processes and sexual conflict, which are very likely to be dependent on ecological factors and specificity of the system studied. For that reason, carefully controlled experiments on laboratory systems and mathematical modelling are necessary steps that should ultimately lead to the study of similar questions in natural systems.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2017. , 40 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1590
Keyword [en]
Sexual selection, Environmental change, Sexual conflict, Environmental stress, Adaptation, Adaptive landscape
National Category
Evolutionary Biology
Research subject
Biology with specialization in Animal Ecology
Identifiers
URN: urn:nbn:se:uu:diva-332119ISBN: 978-91-513-0131-0 (print)OAI: oai:DiVA.org:uu-332119DiVA: diva2:1152253
Public defence
2017-12-15, Lindhalsalen, Norbyväagen 18, 75236, Uppsala, 10:00 (English)
Opponent
Supervisors
Available from: 2017-11-22 Created: 2017-10-24 Last updated: 2017-11-22
List of papers
1. Sex-specific selection under environmental stress in seed beetles
Open this publication in new window or tab >>Sex-specific selection under environmental stress in seed beetles
2017 (English)In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 30, no 1, 161-173 p.Article in journal (Refereed) Published
Abstract [en]

Sexual selection can increase rates of adaptation by imposing strong selection in males, thereby allowing efficient purging of the mutation load on population fitness at a low demographic cost. Indeed, sexual selection tends to be male-biased throughout the animal kingdom, but little empirical work has explored the ecological sensitivity of this sex difference. In this study, we generated theoretical predictions of sex-specific strengths of selection, environmental sensitivities and genotype-by-environment interactions and tested them in seed beetles by manipulating either larval host plant or rearing temperature. Using fourteen isofemale lines, we measured sex-specific reductions in fitness components, genotype-by-environment interactions and the strength of selection (variance in fitness) in the juvenile and adult stage. As predicted, variance in fitness increased with stress, was consistently greater in males than females for adult reproductive success (implying strong sexual selection), but was similar in the sexes in terms of juvenile survival across all levels of stress. Although genetic variance in fitness increased in magnitude under severe stress, heritability decreased and particularly so in males. Moreover, genotype-by-environment interactions for fitness were common but specific to the type of stress, sex and life stage, suggesting that new environments may change the relative alignment and strength of selection in males and females. Our study thus exemplifies how environmental stress can influence the relative forces of natural and sexual selection, as well as concomitant changes in genetic variance in fitness, which are predicted to have consequences for rates of adaptation in sexual populations.

Place, publisher, year, edition, pages
WILEY-BLACKWELL, 2017
Keyword
adaptation, Callosobruchus maculatus, environmental change, host plant, natural selection, population viability, sexual reproduction, sexual selection, stress, temperature
National Category
Zoology Ecology
Identifiers
urn:nbn:se:uu:diva-331971 (URN)10.1111/jeb.12996 (DOI)
Funder
EU, European Research Council, GENCON AdG-294333Swedish Research Council, 621-2010-5266 261-2014-4523
Available from: 2017-10-20 Created: 2017-10-20 Last updated: 2017-10-24Bibliographically approved
2. Intralocus Sexual Conflict and the Tragedy of the Commons in Seed Beetles
Open this publication in new window or tab >>Intralocus Sexual Conflict and the Tragedy of the Commons in Seed Beetles
Show others...
2016 (English)In: American Naturalist, ISSN 0003-0147, E-ISSN 1537-5323, Vol. 188, no 4, E98-E112 p.Article in journal (Refereed) Published
Abstract [en]

The evolution of male traits that inflict direct harm on females during mating interactions can result in a so-called tragedy of the commons, where selfish male strategies depress population viability. This tragedy of the commons can be magnified by intralocus sexual conflict (IaSC) whenever alleles that reduce fecundity when expressed in females spread in the population because of their benefits in males. We evaluated this prediction by detailed phenotyping of 73 isofemale lines of the seed beetle Callosobruchus maculatus. We quantified genetic variation in life history andmorphology, as well as associated covariance in male and female adult reproductive success. In parallel, we created replicated artificial populations of each line and measured their productivity. Genetic constraints limited independent trait expression in the sexes, and we identified several instances of sexually antagonistic covariance between traits and fitness, signifying IaSC. Population productivity was strongly positively correlated to female adult reproductive success but uncorrelated with male reproductive success. Moreover, male (female) phenotypic optima for several traits under sexually antagonistic selection were exhibited by the genotypes with the lowest (highest) population productivity. Our study forms a direct link between individuallevel sex-specific selection and population demography and places lifehistory traits at the epicenter of these dynamics.

Keyword
sexual selection, adaptation, sexual antagonism, sexual dimorphism, genetic architecture, population demography
National Category
Ecology
Identifiers
urn:nbn:se:uu:diva-305304 (URN)10.1086/687963 (DOI)000383774400001 ()27622882 (PubMedID)
Funder
Swedish Research CouncilEU, European Research Council, AdG-294333; AGINGSEXDIFF
Available from: 2016-10-18 Created: 2016-10-14 Last updated: 2017-10-24Bibliographically approved
3. The consequences of sexual selection in well-adapted and amaladapted populations of bean beetles: Sexual selection in maladapted populations
Open this publication in new window or tab >>The consequences of sexual selection in well-adapted and amaladapted populations of bean beetles: Sexual selection in maladapted populations
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Whether sexual selection generally promotes or impedes population persistence remains an open question. Intralocus sexual conflict (IaSC) can render sexual selection in males detrimental to the population by increasing the frequency of alleles with positive effects on male reproductive success but negative effects on female fecundity. Recent modelling based on fitness landscape theory, however, indicates that the relative impact of IaSC may be reduced in maladapted populations and that sexual selection therefore might promote adaptation when it is most needed. Here, we test this prediction using bean beetles that had undergone 80 generations of experimental evolution on two alternative host plants. We isolated and assessed the effect of maladaptation on sex-specific strengths of selection and IaSC by cross-rearing the two experimental evolution regimes on the alternative hosts and estimating within-population genetic (co)variance for fitness in males and females. Two key predictions were upheld: males generally experienced stronger selection compared to females and maladaptation increased selection in females. However, maladaptation consistently decreased male-bias in the strength of selection and IaSC was not reduced in maladapted populations. These findings imply that sexual selection can be disrupted in stressful environmental conditions, thus reducing one of the potential benefits of sexual reproduction in maladapted populations.

National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-331970 (URN)
Available from: 2017-10-20 Created: 2017-10-20 Last updated: 2017-10-24Bibliographically approved
4. The efficiency of purifying sexual selection under environmental change
Open this publication in new window or tab >>The efficiency of purifying sexual selection under environmental change
(English)Manuscript (preprint) (Other academic)
Abstract [en]

Sexual selection can promote adaptation if sexually selected traits are reliable indicators of the bearer’s condition and overall genetic quality. Moreover, stronger sexual selection in males, as often reported in empirical studies, may efficiently purge deleterious alleles at a low cost to population productivity. However, such benefits of sexual selection have been suggested to be compromised during adaptation in a changing environment due to a disruption of the mate choice process. Indeed, substantial insight has been gained from previous theoretical and empirical studies focusing on exploring female choice and the reliability of male sexual signals across environments. In this study, we show that even if sexually selected traits are honest signals and accurately reflect condition in new environments, the efficacy of sexual selection is likely to be reduced under stress. We model the strength of sex-specific selection in a population with males competing among each other for fertilization success and females experiencing fecundity selection. We observe that, for most of the biologically relevant parameter space describing mating system variation, the strength of sexual selection is reduced relatively to fecundity selection as the population becomes increasingly maladapted under environmental change. This result, which is modulated by the characteristics of the mating system, is a direct consequence of the prominent role of social context (frequency-dependence) in sexual selection.

National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-332106 (URN)
Available from: 2017-10-24 Created: 2017-10-24 Last updated: 2017-10-27Bibliographically approved

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Martinossi-Allibert, Ivain

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