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Evolution under increased male postcopulatory sexual selection reduces fertility under heat stress
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology.ORCID iD: 0000-0002-4739-2756
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. Stockholm university.ORCID iD: 0000-0003-3356-7284
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Animal ecology. Martin-Luther University Halle-Wittenberg.ORCID iD: 0000-0002-3433-7248
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(English)Manuscript (preprint) (Other academic)
Abstract [en]

Contemporary climate change is forcing species to rapidly adapt to increasing temperatures. However, in sexually reproducing species, natural and sexual selection may select for different aspects of traits, raising the question whether sexual selection aids or impedes adaptation under climate change. A common expectation is that costly sperm traits, that increase male competitive fertilization success trade off with maintenance effort per gamete. High levels of sperm competition, leading to increased reproductive effort in males, could therefore lead to reduced fertility in stressful environments that put larger demands on gamete maintenance. Here we test this hypothesis by harnessing the empirical potential of long-term experimental evolution in the seed beetle Callosobruchus maculatus. We assessed the thermal sensitivity of fertility (TSF) in replicated lines maintained for 68 generations under three alternative mating regimes, manipulating the opportunity for sexual and natural selection. We find that males from lines that evolved under strong sexual selection show increased TSF, and that male success in sperm competition (P2: sperm offense) is genetically correlated to increased TSF. Direct engagement in male-male competition did, however, not affect the TSF. Interestingly, females from lines under strong sexual selection also showed increased TSF. Since females from these lines experienced relaxed selection on their own reproductive effort, this implies that the female TSF evolved mainly through genetic correlations with selected male traits. We show that transgenerational effects of heat stress are mediated primarily through fathers. These effects are detrimental and reduce offspring fertility, while not affecting offspring TSF (i.e., no evidence for adaptive transgenerational plasticity). Our results suggest that a trade-off between success in post-copulatory sexual selection (sperm competition) and gamete viability can put polyandrous species under immediate risk in the presence of the extreme heat waves expected under future climate change.

National Category
Evolutionary Biology
Identifiers
URN: urn:nbn:se:uu:diva-472979OAI: oai:DiVA.org:uu-472979DiVA, id: diva2:1652966
Available from: 2022-04-20 Created: 2022-04-20 Last updated: 2022-04-27Bibliographically approved
In thesis
1. Condition dependent germline maintenance in seed beetles
Open this publication in new window or tab >>Condition dependent germline maintenance in seed beetles
2022 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The aim of the work presented in this thesis is to investigate how costly adaptations promoted by sexual selection affect fertility and offspring quality through changes in germline maintenance. Germline maintenance, comprising mechanisms maintaining DNA-integrity and homeostasis within germ cells, is known to be costly and, therefore, may trade-off with other costly reproductive traits that are under sexual selection. However, sexual selection may also act on condition dependent traits that reflect the overall genetic quality of its bearer, in which case sexual selection for high quality mates may lead to improved germline maintenance. Using experimental evolution lines of the seed beetle Callosobruchus maculatus, evolving under three different mating regimes that manipulated the opportunity for sexual and natural selection, I show evidence indicating that sexual selection can lead to improved germline maintenance through selection on condition dependent traits. However, I also found evidence for the alternative hypothesis, suggesting that when sexual selection is much stronger than natural selection it may lead to excessive investment into mating traits that trade-off with and reduce germline maintenance. We present an RNA expression analysis suggesting 18 candidate genes responding to DNA-damage and sociosexual interactions that may be involved in trade-offs between sexual selection and germline maintenance. I also found that the fertility of males and females that evolved under intense sexual selection was more sensitive to heat stress, and male sensitivity of fertility to heat stress was genetically correlated to sperm competitive ability. This suggests a trade-off between male postcopulatory reproductive success and the thermal sensitivity of fertility. The increased sensitivity to heat was also reflected in the fertility of females, suggesting that female heat tolerance may have evolved via genetic correlations with sexually selected male reproductive traits. The work presented in this thesis shows that sexual selection indeed affects germline maintenance. Sexual selection can increase germline maintenance through selection on condition dependent traits. But at the same time, traits under sexual selection can trade off with aspects of germline maintenance. If traits evolved under sexual selection and only weak constraints by natural selection, evolved allocation shifts in response to sexual selection can lead to deleterious repercussions when stressful environmental conditions increase demands on germline maintenance. The results presented in this thesis highlight important aspects of how sexual selection affects condition dependent germline maintenance with significant implications for the maintenance of genetic variation, adaptive processes, and mate choice processes in species under sexual selection.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2022. p. 69
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 2155
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-473127 (URN)978-91-513-1512-6 (ISBN)
Public defence
2022-06-13, Friessalen, Norbyvägen 16, Uppsala, 10:00 (English)
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Available from: 2022-05-17 Created: 2022-04-21 Last updated: 2022-06-15

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Baur, JulianZwoinska, MartynaKoppik, MareikeBerger, David

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