Experimental Sexual Selection Affects the Evolution of Physiological and Life-history Traits

Overview

Journal J Evol Biol

Publisher Oxford University Press

Specialty Biology

Date 2022 Apr 6

PMID 35384100

Authors

Martin D Garlovsky

Luke Holman

Andrew L Brooks

Zorana K Novicic

Rhonda R Snook

Affiliations

Soon will be listed here.

Abstract

Sexual selection and sexual conflict are expected to affect all aspects of the phenotype, not only traits that are directly involved in reproduction. Here, we show coordinated evolution of multiple physiological and life-history traits in response to long-term experimental manipulation of the mating system in populations of Drosophila pseudoobscura. Development time was extended under polyandry relative to monogamy in both sexes, potentially due to higher investment in traits linked to sexual selection and sexual conflict. Individuals (especially males) evolving under polyandry had higher metabolic rates and locomotor activity than those evolving under monogamy. Polyandry individuals also invested more in metabolites associated with increased endurance capacity and efficient energy metabolism and regulation, namely lipids and glycogen. Finally, polyandry males were less desiccation- and starvation resistant than monogamy males, suggesting trade-offs between resistance and sexually selected traits. Our results provide experimental evidence that mating systems can impose selection that influences the evolution of non-sexual phenotypes such as development, activity, metabolism and nutrient homeostasis.

Citing Articles

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PMID: 39906580 PMC: 11790217. DOI: 10.1093/evlett/qrae062.

Experimental sexual selection affects the evolution of physiological and life-history traits.

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PMID: 35384100 PMC: 9322299. DOI: 10.1111/jeb.14003.

References

Morimoto J, Wigby S . Differential effects of male nutrient balance on pre- and post-copulatory traits, and consequences for female reproduction in Drosophila melanogaster. Sci Rep. 2016; 6:27673. PMC: 4897696. DOI: 10.1038/srep27673. View

Arnqvist G . Mixed Models Offer No Freedom from Degrees of Freedom. Trends Ecol Evol. 2020; 35(4):329-335. DOI: 10.1016/j.tree.2019.12.004. View

WIGGLESWORTH V . The utilization of reserve substances in Drosophila during flight. J Exp Biol. 1949; 26(2):150-63, illust. DOI: 10.1242/jeb.26.2.150. View

Berson J, Zuk M, Simmons L . Natural and sexual selection on cuticular hydrocarbons: a quantitative genetic analysis. Proc Biol Sci. 2019; 286(1902):20190677. PMC: 6532523. DOI: 10.1098/rspb.2019.0677. View

Hollis B, Keller L, Kawecki T . Sexual selection shapes development and maturation rates in Drosophila. Evolution. 2016; 71(2):304-314. DOI: 10.1111/evo.13115. View

Crudgington H, Fellows S, Snook R . Increased opportunity for sexual conflict promotes harmful males with elevated courtship frequencies. J Evol Biol. 2009; 23(2):440-6. DOI: 10.1111/j.1420-9101.2009.01907.x. View

J Gray L, Simpson S, Polak M . Fruit flies may face a nutrient-dependent life-history trade-off between secondary sexual trait quality, survival and developmental rate. J Insect Physiol. 2017; 104:60-70. DOI: 10.1016/j.jinsphys.2017.11.010. View

Garlovsky M, Holman L, Brooks A, Novicic Z, Snook R . Experimental sexual selection affects the evolution of physiological and life-history traits. J Evol Biol. 2022; 35(5):742-751. PMC: 9322299. DOI: 10.1111/jeb.14003. View

Snook R, Brustle L, Slate J . A test and review of the role of effective population size on experimental sexual selection patterns. Evolution. 2009; 63(7):1923-33. DOI: 10.1111/j.1558-5646.2009.00682.x. View

10.

Marron M, Markow T, Kain K, Gibbs A . Effects of starvation and desiccation on energy metabolism in desert and mesic Drosophila. J Insect Physiol. 2003; 49(3):261-70. DOI: 10.1016/s0022-1910(02)00287-1. View

11.

Long T, Rice W . Adult locomotory activity mediates intralocus sexual conflict in a laboratory-adapted population of Drosophila melanogaster. Proc Biol Sci. 2007; 274(1629):3105-12. PMC: 2293944. DOI: 10.1098/rspb.2007.1140. View

12.

Stangberg J, Immonen E, Moreno P, Bolund E . Experimentally induced intrasexual mating competition and sex-specific evolution in female and male nematodes. J Evol Biol. 2020; 33(12):1677-1688. PMC: 7756511. DOI: 10.1111/jeb.13706. View

13.

Price T, Hodgson D, Lewis Z, Hurst G, Wedell N . Selfish genetic elements promote polyandry in a fly. Science. 2008; 322(5905):1241-3. DOI: 10.1126/science.1163766. View

14.

Cally J, Stuart-Fox D, Holman L . Meta-analytic evidence that sexual selection improves population fitness. Nat Commun. 2019; 10(1):2017. PMC: 6494874. DOI: 10.1038/s41467-019-10074-7. View

15.

Immonen E, Ronn J, Watson C, Berger D, Arnqvist G . Complex mitonuclear interactions and metabolic costs of mating in male seed beetles. J Evol Biol. 2015; 29(2):360-70. DOI: 10.1111/jeb.12789. View

16.

Schielzeth H, Forstmeier W . Conclusions beyond support: overconfident estimates in mixed models. Behav Ecol. 2009; 20(2):416-420. PMC: 2657178. DOI: 10.1093/beheco/arn145. View

17.

Maklakov A, Fricke C, Arnqvist G . Sexual selection affects lifespan and aging in the seed beetle. Aging Cell. 2007; 6(6):739-44. DOI: 10.1111/j.1474-9726.2007.00333.x. View

18.

Wiberg R, Veltsos P, Snook R, Ritchie M . Experimental evolution supports signatures of sexual selection in genomic divergence. Evol Lett. 2021; 5(3):214-229. PMC: 8190450. DOI: 10.1002/evl3.220. View

19.

Veltsos P, Fang Y, Cossins A, Snook R, Ritchie M . Mating system manipulation and the evolution of sex-biased gene expression in Drosophila. Nat Commun. 2017; 8(1):2072. PMC: 5727229. DOI: 10.1038/s41467-017-02232-6. View

20.

Debelle A, Ritchie M, Snook R . Sexual selection and assortative mating: an experimental test. J Evol Biol. 2016; 29(7):1307-16. DOI: 10.1111/jeb.12855. View