Sexual selection, environmental robustness, and evolutionary demography of maladapted populations: A test using experimental evolution in seed beetles

Ivain Martinossi‐Allibert; Emma Thilliez; Göran Arnqvist; David Berger

doi:10.1111/eva.12758

Sexual selection and the evolution of male and female cognition: A test using experimental evolution in seed beetles*

Evolution ◽

10.1111/evo.13793 ◽

2019 ◽

Vol 73 (12) ◽

pp. 2390-2400 ◽

Cited By ~ 4

Author(s):

Julian Baur ◽

Jean d'Amour Nsanzimana ◽

David Berger

Keyword(s):

Sexual Selection ◽

Experimental Evolution ◽

Male And Female ◽

Seed Beetles

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Sexual selection, environmental robustness and evolutionary demography of maladapted populations: a test using experimental evolution in seed beetles

10.1101/426056 ◽

2018 ◽

Cited By ~ 3

Author(s):

Ivain Martinossi-Allibert ◽

Emma Thilliez ◽

Göran Arnqvist ◽

David Berger

Keyword(s):

Sexual Selection ◽

Reproductive Success ◽

Environmental Change ◽

Population Level ◽

Good Genes ◽

Individual Level ◽

Positive Effects ◽

Fecundity Selection ◽

Environmental Robustness ◽

Seed Beetles

AbstractWhether sexual selection impedes or aids adaptation has become a pressing question in times of rapid environmental change and parallels the debate about how the evolution of individual traits impacts on population dynamics and viability. The net effect of sexual selection on population viability results from a balance between genetic benefits of “good genes” effects and costs of sexual conflict. Depending on how these facets of sexual selection are affected under environmental change, extinction of maladapted populations could either be avoided or accelerated. Here, we evolved seed beetles under three alternative mating regimes (polygamy, monogamy and male-limited selection) to disentangle the contributions of sexual selection, fecundity selection and male-female coevolution to individual reproductive success and population fitness. We compared these contributions between the ancestral environment and two new stressful environments (temperature and host plant shift). Evolution under polygamy resulted in the highest individual reproductive success in competitive context for both sexes. Moreover, females evolving only via sexual selection on their male siblings in the male-limited regime had similar reproductive success and higher fertility than females evolving under monogamy, suggesting that sexual selection on males had positive effects on female fitness components. Interestingly, male-limited sexual selection resulted in males that were robust to stress, compared to males from the two evolution regimes applying fecundity selection. We quantified the population-level consequences of this sex-specific adaptation and found evidence that costs of socio-sexual interactions were higher in male-limited lines compared to polygamous lines, and that this difference was particularly pronounced at elevated temperature to which males from the male-limited regime were more robust compared to their conspecific females. These results illustrate the tension between individual-level adaptation and population-level viability in sexually reproducing species and suggest that sex-specific selection can cause differences in environmental robustness that may impact population demography under environmental change.

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Sexual conflict drives micro- and macroevolution of sexual dimorphism in immunity

10.1101/2020.12.20.423717 ◽

2020 ◽

Author(s):

Basabi Bagchi ◽

Quentin Corbel ◽

Imroze Khan ◽

Ellen Payne ◽

Devshuvam Banerji ◽

...

Keyword(s):

Sex Differences ◽

Sexual Selection ◽

Sexual Dimorphism ◽

Mating System ◽

Sexual Conflict ◽

Experimental Evolution ◽

Parasitic Infections ◽

Expression Of Genes ◽

Trade Offs ◽

Seed Beetles

AbstractSexual dimorphism in immunity is believed to reflect sex-differences in trade-offs between competing life history demands. Sexual selection can have major effects on mating rates and sex-specific costs of mating and may thereby influence sex-differences in immunity as well as associated host-pathogen dynamics. Yet, experimental data linking the mating system to evolved sexual dimorphism in immunity are scarce and the direct effects of mating rate on immunity are not well established. Here, we use transcriptomic analyses, experimental evolution and phylogenetic comparative methods to study the association between the mating system and sexual dimorphism in immunity in seed beetles, where mating causes internal injuries in females. We demonstrate that female phenoloxidase (PO) activity, involved in wound healing and defence against parasitic infections, is elevated relative to males as a result of sex-biased expression of genes in the proPO activating cascade. We document substantial phenotypic plasticity in female PO activity in response to mating and show that experimental evolution under enforced monogamy (relative to natural polygamy) rapidly decreases female (but not male) PO activity. The evolution of decreased PO in monogamous females was accompanied by increased tolerance to bacterial infection unrelated to mating. This implies that female responses to costly mating may trade off with other aspects of immune defence. Finally, female (but not male) PO activity show correlated evolution with the perceived harmfulness of male genitalia across 12 species of seed beetles, suggesting that sexual conflict has a significant influence on sexual dimorphisms in immunity in this group of insects. Our results thus provide a proximate and ultimate understanding of the links between sexual selection and sexual dimorphism in immunity.

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Natural selection increases female fitness by reversing the exaggeration of a male sexually selected trait

Nature Communications ◽

10.1038/s41467-021-23804-7 ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Kensuke Okada ◽

Masako Katsuki ◽

Manmohan D. Sharma ◽

Katsuya Kiyose ◽

Tomokazu Seko ◽

...

Keyword(s):

Sexual Selection ◽

Natural Selection ◽

Experimental Evolution ◽

Genetic Correlations ◽

Lifetime Reproductive Success ◽

Fundamental Theory ◽

Female Fitness ◽

Male Trait ◽

Flour Beetles ◽

Male Specific

AbstractTheory shows how sexual selection can exaggerate male traits beyond naturally selected optima and also how natural selection can ultimately halt trait elaboration. Empirical evidence supports this theory, but to our knowledge, there have been no experimental evolution studies directly testing this logic, and little examination of possible associated effects on female fitness. Here we use experimental evolution of replicate populations of broad-horned flour beetles to test for effects of sex-specific predation on an exaggerated sexually selected male trait (the mandibles), while also testing for effects on female lifetime reproductive success. We find that populations subjected to male-specific predation evolve smaller sexually selected mandibles and this indirectly increases female fitness, seemingly through intersexual genetic correlations we document. Predation solely on females has no effects. Our findings support fundamental theory, but also reveal unforseen outcomes—the indirect effect on females—when natural selection targets sex-limited sexually selected characters.

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Sexual conflict drives micro- and macroevolution of sexual dimorphism in immunity

BMC Biology ◽

10.1186/s12915-021-01049-6 ◽

2021 ◽

Vol 19 (1) ◽

Author(s):

Basabi Bagchi ◽

Quentin Corbel ◽

Imroze Khan ◽

Ellen Payne ◽

Devshuvam Banerji ◽

...

Keyword(s):

Sex Differences ◽

Sexual Dimorphism ◽

Mating System ◽

Sexual Conflict ◽

Experimental Evolution ◽

Parasitic Infections ◽

Pathogen Dynamics ◽

Trade Offs ◽

Host Pathogen ◽

Seed Beetles

Abstract Background Sexual dimorphism in immunity is believed to reflect sex differences in reproductive strategies and trade-offs between competing life history demands. Sexual selection can have major effects on mating rates and sex-specific costs of mating and may thereby influence sex differences in immunity as well as associated host–pathogen dynamics. Yet, experimental evidence linking the mating system to evolved sexual dimorphism in immunity are scarce and the direct effects of mating rate on immunity are not well established. Here, we use transcriptomic analyses, experimental evolution and phylogenetic comparative methods to study the association between the mating system and sexual dimorphism in immunity in seed beetles, where mating causes internal injuries in females. Results We demonstrate that female phenoloxidase (PO) activity, involved in wound healing and defence against parasitic infections, is elevated relative to males. This difference is accompanied by concomitant sex differences in the expression of genes in the prophenoloxidase activating cascade. We document substantial phenotypic plasticity in female PO activity in response to mating and show that experimental evolution under enforced monogamy (resulting in low remating rates and reduced sexual conflict relative to natural polygamy) rapidly decreases female (but not male) PO activity. Moreover, monogamous females had evolved increased tolerance to bacterial infection unrelated to mating, implying that female responses to costly mating may trade off with other aspects of immune defence, an hypothesis which broadly accords with the documented sex differences in gene expression. Finally, female (but not male) PO activity shows correlated evolution with the perceived harmfulness of male genitalia across 12 species of seed beetles, suggesting that sexual conflict has a significant influence on sexual dimorphisms in immunity in this group of insects. Conclusions Our study provides insights into the links between sexual conflict and sexual dimorphism in immunity and suggests that selection pressures moulded by mating interactions can lead to a sex-specific mosaic of immune responses with important implications for host–pathogen dynamics in sexually reproducing organisms.

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Sexual selection and experimental evolution of chemical signals inDrosophila pseudoobscura

Journal of Evolutionary Biology ◽

10.1111/j.1420-9101.2012.02603.x ◽

2012 ◽

Vol 25 (11) ◽

pp. 2232-2241 ◽

Cited By ~ 17

Author(s):

J. Hunt ◽

R. R. Snook ◽

C. Mitchell ◽

H. S. Crudgington ◽

A. J. Moore

Keyword(s):

Sexual Selection ◽

Experimental Evolution ◽

Chemical Signals

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Sexual selection and the evolution of male and female cognition: a test using experimental evolution in seed beetles

10.1101/514711 ◽

2019 ◽

Author(s):

Julian Baur ◽

Jean d’Amour ◽

David Berger

Keyword(s):

Sexual Selection ◽

Cognitive Abilities ◽

Balancing Selection ◽

Experimental Studies ◽

Good Genes ◽

Human Cognition ◽

Potential Force ◽

Sexual Selection Theory ◽

Rate Of Learning ◽

Seed Beetles

Abstract“The mating mind hypothesis”, originally aimed at explaining human cognition, holds that the socio-sexual environment shapes cognitive abilities among animals. Similarly, general sexual selection theory predicts that mate competition should benefit individuals carrying “good genes” with beneficial pleiotropic effects on general cognitive ability. However, few experimental studies have evaluated these related hypotheses due to difficulties of performing direct tests in most taxa. Here we harnessed the empirical potential of the seed beetle study system to investigate the role of sexual selection and mating system in the evolution of cognition. We evolved replicate lines of beetle under enforced monogamy (eliminating sexual selection) or polygamy for 35 generations and then challenged them to locate and discriminate among mating partners (male assays) or host seeds (female assays). To assess learning, the same beetles performed the task in three consecutive rounds. All lines learned the task, improving both within and between trails. Moreover, polygamous males outperformed monogamous males. However, there were no differences in the rate of learning between males of the two regimes, and polygamous females showed no improvement in host search, and even signs of reduced learning. Hence, while sexual selection was a potent factor that increased cognitive performance in mate search, it did not lead to the general increase in cognitive abilities expected under the “mating mind” hypothesis or general “good genes” theory. Our results highlight sexually antagonistic (balancing) selection as a potential force maintaining genetic variation in cognitive traits.

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Sexual selection and inbreeding: two efficient ways to limit the accumulation of deleterious mutations

10.1101/273367 ◽

2018 ◽

Cited By ~ 2

Author(s):

E. Noël ◽

E. Fruitet ◽

D. Lelaurin ◽

N. Bonel ◽

A. Ségard ◽

...

Keyword(s):

Sexual Selection ◽

Experimental Evolution ◽

Genetic Load ◽

Deleterious Mutations ◽

Mutation Load ◽

Male Function ◽

Female Function ◽

Deleterious Alleles ◽

Self Fertilization ◽

Male Specific

AbstractTheory and empirical data showed that two processes can boost selection against deleterious mutations, thus facilitating the purging of the mutation load: inbreeding, by exposing recessive deleterious alleles to selection in homozygous form, and sexual selection, by enhancing the relative reproductive success of males with small mutation loads. These processes tend to be mutually exclusive because sexual selection is reduced under mating systems that promote inbreeding, such as self-fertilization in hermaphrodites. We estimated the relative efficiency of inbreeding and sexual selection at purging the genetic load, using 50 generations of experimental evolution, in a hermaphroditic snail (Physa acuta). To this end, we generated lines that were exposed to various intensities of inbreeding, sexual selection (on the male function) and nonsexual selection (on the female function). We measured how these regimes affected the mutation load, quantified through the survival of outcrossed and selfed juveniles. We found that juvenile survival strongly decreased in outbred lines with reduced male selection, but not when female selection was relaxed, showing that male-specific sexual selection does purge deleterious mutations. However, in lines exposed to inbreeding, where sexual selection was also relaxed, survival did not decrease, and even increased for self-fertilized juveniles, showing that purging through inbreeding can compensate for the absence of sexual selection. Our results point to the further question of whether a mixed strategy combining the advantages of both mechanisms of genetic purging could be evolutionary stable.

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Can Sexual Selection Cause Divergence in Mating System-Related Floral Traits?

10.1101/513481 ◽

2019 ◽

Author(s):

Åsa Lankinen ◽

Maria Strandh

Keyword(s):

Sexual Selection ◽

Mating System ◽

Experimental Evolution ◽

Seed Set ◽

Pollen Competition ◽

Floral Traits ◽

Mixed Mating ◽

Stigma Receptivity ◽

Source Line ◽

Outcrossing Species

AbstractPremise of the ResearchThe wide diversity of floral traits seen among plants is shaped by neutral and selective evolutionary processes. In outcrossing species, sexual selection from competing pollen donors is expected to be important for shaping mating system-related traits but empirical evidence is scarce. In a previous evaluation of experimental evolution lines crossed with either one or two pollen donors (monogamous, M, or polyandrous, P, lines) at early floral stages in mixed-mating Collinsia heterophylla (Plantaginaceae), P showed enhanced pollen competitive ability and reduced maternal seed set compared to M, in accordance with sexually antagonistic evolution of pollen. Here, we asked whether the presence of sexual selection during pollen competition affect mating system-related floral traits in the same lines.MethodologyWe compared flowering start, timing of anther-stigma contact (as an indication of timing of self-pollination), timing of stigma receptivity and first seed set between M and P, and with a source line, S (starting material). The former three traits are later in outcrossers than in selfers of Collinsia. The latter trait was expected to be earlier in P than in M because of sexual selection for early seed siring of pollen.Pivotal ResultsArtificial polyandry for four generations resulted in later flowering start and later anther-stigma contact in P compared to M, and the latter trait was intermediate in S. Thus, P appeared more ‘outcrossing’ than M. Stigma receptivity did not differ between lines. First seed set was earlier in P than in M, as expected from sexual selection.ConclusionsOur results from C. heterophylla experimental evolution lines suggest that a component of sexual selection during outcross pollination could enhance the patterns of floral divergence commonly found between outcrossers and selfers.

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