| 1. |
- Baur, Julian, et al.
(författare)
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Coevolution of longevity and female germline maintenance
- 2024
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Ingår i: Proceedings of the Royal Society of London. Biological Sciences. - : Royal Society. - 0962-8452 .- 1471-2954. ; 291:2024
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Tidskriftsartikel (refereegranskat)abstract
- An often-overlooked aspect of life-history optimization is the allocation of resources to protect the germline and secure safe transmission of genetic information. While failure to do so renders significant fitness consequences in future generations, germline maintenance comes with substantial costs. Thus, germline allocation should trade off with other life-history decisions and be optimized in accordance with an organism's reproductive schedule. Here, we tested this hypothesis by studying germline maintenance in lines of seed beetle, selected for early (E) or late (L) reproduction for 350 and 240 generations, respectively. Female animals provide maintenance and screening of male gametes in their reproductive tract and oocytes. Here, we reveal the ability of young and aged E- and L-females to provide this form of germline maintenance by mating them to males with ejaculates with artificially elevated levels of protein and DNA damage. We find that germline maintenance in E-females peaks at young age and then declines, while the opposite is true for L-females, in accordance with the age of reproduction in the respective regime. These findings identify the central role of allocation to secure germline integrity in life-history evolution and highlight how females can play a crucial role in mitigating the effects of male germline decisions on mutation rate and offspring quality.
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| 2. |
- Baur, Julian, et al.
(författare)
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Evolution under increased male postcopulatory sexual selection reduces fertility under heat stress
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Annan publikation (övrigt vetenskapligt/konstnärligt)abstract
- 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.
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| 3. |
- Baur, Julian, et al.
(författare)
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Heat stress reveals a fertility debt owing to postcopulatory sexual selection
- 2023
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Ingår i: Evolution Letters. - : Oxford University Press (OUP). - 2056-3744. ; 8:1, s. 101-113
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Tidskriftsartikel (refereegranskat)abstract
- Climates are changing rapidly, demanding equally rapid adaptation of natural populations. Whether sexual selection can aid such adaptation is under debate; while sexual selection should promote adaptation when individuals with high mating success are also best adapted to their local surroundings, the expression of sexually selected traits can incur costs. Here we asked what the demographic consequences of such costs may be once climates change to become harsher and the strength of natural selection increases. We first adopted a classic life history theory framework, incorporating a trade-off between reproduction and maintenance, and applied it to the male germline to generate formalized predictions for how an evolutionary history of strong postcopulatory sexual selection (sperm competition) may affect male fertility under acute adult heat stress. We then tested these predictions by assessing the thermal sensitivity of fertility (TSF) in replicated lineages of seed beetles maintained for 68 generations under three alternative mating regimes manipulating the opportunity for sexual and natural selection. In line with the theoretical predictions, we find that males evolving under strong sexual selection suffer from increased TSF. Interestingly, females from the regime under strong sexual selection, who experienced relaxed selection on their own reproductive effort, had high fertility in benign settings but suffered increased TSF, like their brothers. This implies that female fertility and TSF evolved through genetic correlation with reproductive traits sexually selected in males. Paternal but not maternal heat stress reduced offspring fertility with no evidence for adaptive transgenerational plasticity among heat-exposed offspring, indicating that the observed effects may compound over generations. Our results suggest that trade-offs between fertility and traits increasing success in postcopulatory sexual selection can be revealed in harsh environments. This can put polyandrous species under immediate risk during extreme heat waves expected under future climate change.
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| 4. |
- Baur, Julian, et al.
(författare)
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Heat stress reveals a fertility debt owing to postcopulatory sexual selection
- 2024
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Ingår i: Evolution Letters. - : Oxford University Press. - 2056-3744. ; 8:1, s. 101-113
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Tidskriftsartikel (refereegranskat)abstract
- Climates are changing rapidly, demanding equally rapid adaptation of natural populations. Whether sexual selection can aid such adaptation is under debate; while sexual selection should promote adaptation when individuals with high mating success are also best adapted to their local surroundings, the expression of sexually selected traits can incur costs. Here we asked what the demographic consequences of such costs may be once climates change to become harsher and the strength of natural selection increases. We first adopted a classic life history theory framework, incorporating a trade-off between reproduction and maintenance, and applied it to the male germline to generate formalized predictions for how an evolutionary history of strong postcopulatory sexual selection (sperm competition) may affect male fertility under acute adult heat stress. We then tested these predictions by assessing the thermal sensitivity of fertility (TSF) in replicated lineages of seed beetles maintained for 68 generations under three alternative mating regimes manipulating the opportunity for sexual and natural selection. In line with the theoretical predictions, we find that males evolving under strong sexual selection suffer from increased TSF. Interestingly, females from the regime under strong sexual selection, who experienced relaxed selection on their own reproductive effort, had high fertility in benign settings but suffered increased TSF, like their brothers. This implies that female fertility and TSF evolved through genetic correlation with reproductive traits sexually selected in males. Paternal but not maternal heat stress reduced offspring fertility with no evidence for adaptive transgenerational plasticity among heat-exposed offspring, indicating that the observed effects may compound over generations. Our results suggest that trade-offs between fertility and traits increasing success in postcopulatory sexual selection can be revealed in harsh environments. This can put polyandrous species under immediate risk during extreme heat waves expected under future climate change.
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| 5. |
- Baur, Julian, et al.
(författare)
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The mating system affects the temperature sensitivity of male and female fertility
- 2022
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Ingår i: Functional Ecology. - : John Wiley & Sons. - 0269-8463 .- 1365-2435. ; 36:1, s. 92-106
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Tidskriftsartikel (refereegranskat)abstract
- To mitigate the effects of climate change, it is important to understand species' responses to increasing temperatures. This has often been done by studying survival or activity at temperature extremes. Before such extremes are reached, however, effects on fertility may already be apparent.Sex differences in the thermal sensitivity of fertility (TSF) could impact species persistence under climate warming because female fertility is typically more limiting to population growth than male fertility. However, little is known about sex differences in TSF.Here we first demonstrate that the mating system can strongly influence TSF using the seed beetle Callosobruchus maculatus. We exposed populations carrying artificially induced mutations to two generations of short-term experimental evolution under alternative mating systems, manipulating the opportunity for natural and sexual selection on the mutations. We then measured TSF in males and females subjected to juvenile or adult heat stress.Populations kept under natural and sexual selection had higher fitness, but similar TSF, compared to control populations kept under relaxed selection. However, females had higher TSF than males, and strikingly, this sex difference had increased over only two generations in populations evolving under sexual selection.We hypothesized that an increase in male-induced harm to females during mating had played a central role in driving this evolved sex difference, and indeed, remating under conditions limiting male harassment of females reduced both male and female TSF. Moreover, we show that manipulation of mating system parameters in C. maculatus generates intraspecific variation in the sex difference in TSF equal to that found among a diverse set of studies on insects.Our study provides a causal link between the mating system and TSF. Sexual conflict, (re)mating rates and genetic responses to sexual selection differ among ecological settings, mating systems and species. Our study therefore also provides mechanistic understanding for the variability in previously reported TSFs which can inform future experimental assays and predictions of species responses to climate warming.
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| 6. |
- Dougherty, Liam R., et al.
(författare)
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A systematic map of studies testing the relationship between temperature and animal reproduction
- 2024
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Ingår i: Ecological Solutions and Evidence. - : John Wiley & Sons. - 2688-8319. ; 5:1
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Tidskriftsartikel (refereegranskat)abstract
- Exposure to extreme temperatures can negatively affect animal reproduction, by disrupting the ability of individuals to produce any offspring (fertility), or the number of offspring produced by fertile individuals (fecundity). This has important ecological consequences, because reproduction is the ultimate measure of population fitness: a reduction in reproductive output lowers the population growth rate and increases the extinction risk. Despite this importance, there have been no large-scale summaries of the evidence for effect of temperature on reproduction.We provide a systematic map of studies testing the relationship between temperature and animal reproduction. We systematically searched for published studies that statistically test for a direct link between temperature and animal reproduction, in terms of fertility, fecundity or indirect measures of reproductive potential (gamete and gonad traits).Overall, we collated a large and rich evidence base, with 1654 papers that met our inclusion criteria, encompassing 1191 species.The map revealed several important research gaps. Insects made up almost half of the dataset, but reptiles and amphibians were uncommon, as were non-arthropod invertebrates. Fecundity was the most common reproductive trait examined, and relatively few studies measured fertility. It was uncommon for experimental studies to test exposure of different life stages, exposure to short-term heat or cold shock, exposure to temperature fluctuations, or to independently assess male and female effects. Studies were most often published in journals focusing on entomology and pest control, ecology and evolution, aquaculture and fisheries science, and marine biology. Finally, while individuals were sampled from every continent, there was a strong sampling bias towards mid-latitudes in the Northern Hemisphere, such that the tropics and polar regions are less well sampled.This map reveals a rich literature of studies testing the relationship between temperature and animal reproduction, but also uncovers substantial missing treatment of taxa, traits, and thermal regimes. This database will provide a valuable resource for future quantitative meta-analyses, and direct future studies aiming to fill identified gaps.
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| 7. |
- Koppik, Mareike, et al.
(författare)
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Egg laying rather than host quality or host feeding experience drives habitat estimation in the parasitic wasp Nasonia vitripennis
- 2019
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Ingår i: Ecology and Evolution. - : WILEY. - 2045-7758. ; 9:24, s. 14015-14022
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Tidskriftsartikel (refereegranskat)abstract
- In variable environments, sampling information on habitat quality is essential for making adaptive foraging decisions. In insect parasitoids, females foraging for hosts have repeatedly been shown to employ behavioral strategies that are in line with predictions from optimal foraging models. Yet, which cues exactly are employed to sample information on habitat quality has rarely been investigated. Using the gregarious parasitoid Nasonia vitripennis (Walker; Hymenoptera: Pteromalidae), we provided females with different cues about hosts to elucidate, which of them would change a wasp's posterior behavior suggesting a change in information status. We employed posterior clutch size decisions on a host as proxy for a female's estimation of habitat quality. Taking into account changes in physiological state of the foraging parasitoid, we tested whether different host qualities encountered previously change the subsequent clutch size decision in females. Additionally, we investigated whether other kinds of positive experiences-such as ample time to investigate hosts, host feeding, or egg laying-would increase a wasp's estimated value of habitat quality. Contrary to our expectations, quality differences in previously encountered hosts did not affect clutch size decisions. However, we found that prior egg laying experience changes posterior egg allocation to a host, indicating a change in female information status. Host feeding and the time available for host inspection, though correlated with egg laying experience, did not seem to contribute to this change in information status.
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| 8. |
- Koppik, Mareike, et al.
(författare)
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Increased male investment in sperm competition results in reduced maintenance of gametes
- 2023
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Ingår i: PLoS biology. - : Public Library of Science (PLoS). - 1544-9173 .- 1545-7885. ; 21:4
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Tidskriftsartikel (refereegranskat)abstract
- Male animals often show higher mutation rates than their female conspecifics. A hypothesis for this male bias is that competition over fertilization of female gametes leads to increased male investment into reproduction at the expense of maintenance and repair, resulting in a trade-off between male success in sperm competition and offspring quality. Here, we provide evidence for this hypothesis by harnessing the power of experimental evolution to study effects of sexual selection on the male germline in the seed beetle Callosobruchus maculatus.We first show that 50 generations of evolution under strong sexual selection, coupled with experimental removal of natural selection, resulted in males that are more successful in sperm competition. We then show that these males produce progeny of lower quality if engaging in sociosexual interactions prior to being challenged to surveil and repair experimentally induced damage in their germline and that the presence of male competitors alone can be enough to elicit this response. We identify 18 candidate genes that showed differential expression in response to the induced germline damage, with several of these previously implicated in processes associated with DNA repair and cellular maintenance. These genes also showed significant expression changes across sociosexual treatments of fathers and predicted the reduction in quality of their offspring, with expression of one gene also being strongly correlated to male sperm competition success. Sex differences in expression of the same 18 genes indicate a substantially higher female investment in germline maintenance.While more work is needed to detail the exact molecular underpinnings of our results, our findings provide rare experimental evidence for a trade-off between male success in sperm competition and germline maintenance. This suggests that sex differences in the relative strengths of sexual and natural selection are causally linked to male mutation bias. The tenet advocated here, that the allocation decisions of an individual can affect plasticity of its germline and the resulting genetic quality of subsequent generations, has several interesting implications for mate choice processes.
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