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1.
  • Dougherty, Liam R., et al. (author)
  • A systematic map of studies testing the relationship between temperature and animal reproduction
  • 2024
  • In: Ecological Solutions and Evidence. - : John Wiley & Sons. - 2688-8319. ; 5:1
  • Journal article (peer-reviewed)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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2.
  • Parratt, Steven R., et al. (author)
  • Temperatures that sterilize males better match global species distributions than lethal temperatures
  • 2021
  • In: Nature Climate Change. - : Springer Science and Business Media LLC. - 1758-678X .- 1758-6798. ; 11:6
  • Journal article (peer-reviewed)abstract
    • Attempts to link physiological thermal tolerance to global species distributions have relied on lethal temperature limits, yet many organisms lose fertility at sublethal temperatures. Here we show that, across 43 Drosophila species, global distributions better match male-sterilizing temperatures than lethal temperatures. This suggests that species distributions may be determined by thermal limits to reproduction, not survival, meaning we may be underestimating the impacts of climate change for many organisms.
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3.
  • Rodrigues, Leonor R., et al. (author)
  • The genetic basis and adult reproductive consequences of developmental thermal plasticity
  • 2022
  • In: Journal of Animal Ecology. - : Wiley. - 0021-8790 .- 1365-2656. ; 91:6, s. 1119-1134
  • Journal article (peer-reviewed)abstract
    • Increasing temperature and thermal variability generate profound selection on populations. Given the fast rate of environmental change, understanding the role of plasticity and genetic adaptation in response to increasing temperatures is critical. This may be especially true for thermal effects on reproductive traits in which thermal fertility limits at high temperatures may be lower than for survival traits. Consequences of changing environments during development on adult phenotypes may be particularly problematic for core traits such as reproduction that begin early in development. Here we examine the consequences of developmental thermal plasticity on subsequent adult reproductive traits and its genetic basis.We used a panel of Drosophila melanogaster (the Drosophila Genetic Reference Panel; DGRP) in which male fertility performance was previously defined as either showing relatively little (status = ‘high’-performing lines) or substantial (‘low’-performing lines) decline when exposed to increasing developmental temperatures. We used a thermal reaction norm approach to quantify variation in the consequences of developmental thermal plasticity on multiple adult reproductive traits, including sex-specific responses, and to identify candidate genes underlying such variation.Developmental thermal stress impacted the means and thermal reaction norms of all reproductive traits except offspring sex ratio. Mating success declined as temperature increased with no difference between high and low lines, whereas increasing temperature resulted in declines for both male and female fertility and productivity but depended on line status. Fertility and offspring number were positively correlated within and between the sexes across lines, but males were more affected than females.We identified 933 SNPs with significant evolved genetic differentiation between high and low lines. In all, 54 of these lie within genomic windows of overall high differentiation, have significant effects of genotype on the male thermal reaction norm for productivity and are associated with 16 genes enriched for phenotypes affecting reproduction, stress responses and autophagy in Drosophila and other organisms.Our results illustrate considerable plasticity in male thermal limits on several reproductive traits following development at high temperature, and we identify differentiated loci with relevant phenotypic effects that may contribute to this population variation. While our work is on a single population, phenotypic results align with an increasing number of studies demonstrating the potential for stronger selection of thermal stress on reproductive traits, particularly in males. Such large fitness costs may have both short- and long-term consequences for the evolution of populations in response to a warming world.
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4.
  • Walsh, Benjamin S., et al. (author)
  • Female fruit flies cannot protect stored sperm from high temperature damage
  • 2022
  • In: Journal of Thermal Biology. - : Elsevier BV. - 0306-4565 .- 1879-0992. ; 105
  • Journal article (peer-reviewed)abstract
    • Recently, it has been demonstrated that heat-induced male sterility is likely to shape population persistence as climate change progresses. However, an under-explored possibility is that females may be able to successfully store and preserve sperm at temperatures that sterilise males, which could ameliorate the impact of male infertility on populations. Here, we test whether females from two fruit fly species can protect stored sperm from a high temperature stress. We find that sperm carried by female Drosophila virilis are almost completely sterilised by high temperatures, whereas sperm carried by female Zaprionus indianus show only slightly reduced fertility. Heat-shocked D. virilis females can recover fertility when allowed to remate, suggesting that the delivered heat-shock is damaging stored sperm and not directly damaging females in this species. The temperatures required to reduce fertility of mated females are substantially lower than the temperatures required to damage mature sperm in males, suggesting that females are worse than males at protecting mature sperm. This suggests that female sperm storage is unlikely to ameliorate the impacts of high temperature fertility losses in males, and instead exacerbates fertility costs of high temperatures, representing an important determinant of population persistence during climate change.
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5.
  • Walsh, Benjamin S., et al. (author)
  • Plastic responses of survival and fertility following heat stress in pupal and adult Drosophila virilis
  • 2021
  • In: Ecology and Evolution. - : Wiley. - 2045-7758. ; 11:24, s. 18238-18247
  • Journal article (peer-reviewed)abstract
    • The impact of rising global temperatures on survival and reproduction is putting many species at risk of extinction. In particular, it has recently been shown that thermal effects on reproduction, especially limits to male fertility, can underpin species distributions in insects. However, the physiological factors influencing fertility at high temperatures are poorly understood. Key factors that affect somatic thermal tolerance such as hardening, the ability to phenotypically increase thermal tolerance after a mild heat shock, and the differential impact of temperature on different life stages are largely unexplored for thermal fertility tolerance. Here, we examine the impact of high temperatures on male fertility in the cosmopolitan fruit fly Drosophila virilis. We first determined whether temperature stress at either the pupal or adult life history stage impacts fertility. We then tested the capacity for heat-hardening to mitigate heat-induced sterility. We found that thermal stress reduces fertility in different ways in pupae and adults. Pupal heat stress delays sexual maturity, whereas males heated as adults can reproduce initially following heat stress, but become sterile within seven days. We also found evidence that while heat-hardening in D. virilis can improve high temperature survival, there is no significant protective impact of this same hardening treatment on fertility. These results suggest that males may be unable to prevent the costs of high temperature stress on fertility through heat-hardening, which limits a species' ability to quickly and effectively reduce fertility loss in the face of short-term high temperature events.
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6.
  • Walsh, Benjamin S., et al. (author)
  • The Impact of Climate Change on Fertility
  • 2019
  • In: Trends in Ecology & Evolution. - : Elsevier BV. - 0169-5347 .- 1872-8383. ; 34:3, s. 249-259
  • Research review (peer-reviewed)abstract
    • Rising global temperatures are threatening biodiversity. Studies on the impact of temperature on natural populations usually use lethal or viability thresholds, termed the 'critical thermal limit' (CTL). However, this overlooks important sublethal impacts of temperature that could affect species' persistence. Here we discuss a critical but overlooked trait: fertility, which can deteriorate at temperatures less severe than an organism's lethal limit. We argue that studies examining the ecological and evolutionary impacts of climate change should consider the 'thermal fertility limit' (TFL) of species; we propose that a framework for the design of TFL studies across taxa be developed. Given the importance of fertility for population persistence, understanding how climate change affects TFLs is vital for the assessment of future biodiversity impacts.
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7.
  • Bretman, Amanda, et al. (author)
  • Systematic approaches to assessing high-temperature limits to fertility in animals
  • 2024
  • In: Journal of Evolutionary Biology. - 1010-061X .- 1420-9101.
  • Journal article (peer-reviewed)abstract
    • Critical thermal limits (CTLs) gauge the physiological impact of temperature on survival or critical biological function, aiding predictions of species range shifts and climatic resilience. Two recent Drosophila species studies, using similar approaches to determine temperatures that induce sterility (thermal fertility limits [TFLs]), reveal that TFLs are often lower than CTLs and that TFLs better predict both current species distributions and extinction probability. Moreover, many studies show fertility is more sensitive at less extreme temperatures than survival (thermal sensitivity of fertility [TSF]). These results present a more pessimistic outlook on the consequences of climate change. However, unlike CTLs, TFL data are limited to Drosophila, and variability in TSF methods poses challenges in predicting species responses to increasing temperature. To address these data and methodological gaps, we propose 3 standardized approaches for assessing thermal impacts on fertility. We focus on adult obligate sexual terrestrial invertebrates but also provide modifications for other animal groups and life-history stages. We first outline a gold-standard protocol for determining TFLs, focussing on the effects of short-term heat shocks and simulating more frequent extreme heat events predicted by climate models. As this approach may be difficult to apply to some organisms, we then provide a standardized TSF protocol. Finally, we provide a framework to quantify fertility loss in response to extreme heat events in nature, given the limitations in laboratory approaches. Applying these standardized approaches across many taxa, similar to CTLs, will allow robust tests of the impact of fertility loss on species responses to increasing temperatures. Graphical AbstractOverview of the systematic methods (A, C, and D) to simultaneously assay lethal limits and thermal fertility limits or (B and E) thermal sensitivity of fertility. These are most easily applied to laboratory settings but can be used for assessing the fertility of wild-caught animals that have been exposed to natural temperatures.
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8.
  • Rodrigues, Leonor R., et al. (author)
  • Fluctuating heat stress during development exposes reproductive costs and putative benefits
  • 2022
  • In: Journal of Animal Ecology. - : Wiley. - 0021-8790 .- 1365-2656. ; 91:2, s. 391-403
  • Journal article (peer-reviewed)abstract
    • Temperature and thermal variability are increasing worldwide, with well-known survival consequences. However, effects on other potentially more thermally sensitive reproductive traits are less understood, especially when considering thermal variation. Studying the consequences of male reproduction in the context of climate warming and ability to adapt is becoming increasingly relevant.Our goals were to test how exposure to different average temperatures that either fluctuated or remained constant impacts different male reproductive performance traits and to assess adaptive potential to future heat stress.We took advantage of a set of Drosophila melanogaster isogenic lines of different genotypes, exposing them to four different thermal conditions. These conditions represented a benign and a stressful mean temperature, applied either constantly or fluctuating around the mean and experienced during development when heat stress avoidance is hindered because of restricted mobility. We measured subsequent male reproductive performance for mating success, fertility, number of offspring produced and offspring sex ratio, and calculated the influence of thermal stress on estimated heritability and evolvability of these reproductive traits.Both costs and benefits to different thermal conditions on reproductive performance were found, with some responses varying between genotypes. Mating success improved under fluctuating benign temperature conditions and declined as temperature stress increased regardless of genotype. Fertility and productivity were severely reduced at fluctuating mean high temperature for all genotypes, but some genotypes were unaffected at constant high mean temperature. These more thermally robust genotypes showed a slight increase in productivity under the fluctuating benign condition compared to constant high temperature, despite both thermal conditions sharing the same temperature for 6 hr daily. Increasing thermal stress resulted in higher heritability and evolvability.Overall, the effects of temperature on reproductive performance depended on the trait and genotype; performance of some traits slightly increased when high temperatures were experienced for short periods but decreased substantially even when experiencing a benign temperature for a portion of each day. While thermal stress increased genetic variation that could provide adaptive potential against climate warming, this is unlikely to compensate for the overall severe negative effect on reproductive performance as mean temperature and variance increase.
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9.
  • Veltsos, Paris, et al. (author)
  • Experimental sexual selection reveals rapid evolutionary divergence in sex-specific transcriptomes and their interactions following mating
  • 2022
  • In: Molecular Ecology. - : Wiley. - 0962-1083 .- 1365-294X. ; 31:12, s. 3374-3388
  • Journal article (peer-reviewed)abstract
    • Post copulatory interactions between the sexes in internally fertilizing species elicits both sexual conflict and sexual selection. Macroevolutionary and comparative studies have linked these processes to rapid transcriptomic evolution in sex-specific tissues and substantial transcriptomic post mating responses in females, patterns of which are altered when mating between reproductively isolated species. Here, we tested multiple predictions arising from sexual selection and conflict theory about the evolution of sex-specific and tissue-specific gene expression and the post mating response at the microevolutionary level. Following over 150 generations of experimental evolution under either reduced (enforced monogamy) or elevated (polyandry) sexual selection in Drosophila pseudoobscura, we found a substantial effect of sexual selection treatment on transcriptomic divergence in virgin male and female reproductive tissues (testes, male accessory glands, the female reproductive tract and ovaries). Sexual selection treatment also had a dominant effect on the post mating response, particularly in the female reproductive tract - the main arena for sexual conflict - compared to ovaries. This effect was asymmetric with monandry females typically showing more post mating responses than polyandry females, with enriched gene functions varying across treatments. The evolutionary history of the male partner had a larger effect on the post mating response of monandry females, but females from both sexual selection treatments showed unique patterns of gene expression and gene function when mating with males from the alternate treatment. Our microevolutionary results mostly confirm comparative macroevolutionary predictions on the role of sexual selection on transcriptomic divergence and altered gene regulation arising from divergent coevolutionary trajectories between sexual selection treatments.
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10.
  • Veltsos, Paris, et al. (author)
  • Mating system manipulation and the evolution of sex-biased gene expression in Drosophila
  • 2017
  • In: Nature Communications. - : Springer Science and Business Media LLC. - 2041-1723. ; 8
  • Journal article (peer-reviewed)abstract
    • Sex differences in dioecious animals are pervasive and result from gene expression differences. Elevated sexual selection has been predicted to increase the number and expression of male-biased genes, and experimentally imposing monogamy on Drosophila melanogaster has led to a relative feminisation of the transcriptome. Here, we test this hypothesis further by subjecting another polyandrous species, D. pseudoobscura, to 150 generations of experimental monogamy or elevated polyandry. We find that sex-biased genes do change in expression but, contrary to predictions, there is usually masculinisation of the transcriptome under monogamy, although this depends on tissue and sex. We also identify and describe gene expression changes following courtship experience. Courtship often influences gene expression, including patterns in sex-biased gene expression. Our results confirm that mating system manipulation disproportionately influences sex-biased gene expression but show that the direction of change is dynamic and unpredictable.
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11.
  • Wiberg, R. Axel W., et al. (author)
  • Experimental evolution supports signatures of sexual selection in genomic divergence
  • 2021
  • In: Evolution Letters. - : Oxford University Press (OUP). - 2056-3744. ; 5:3, s. 214-229
  • Journal article (peer-reviewed)abstract
    • Comparative genomics has contributed to the growing evidence that sexual selection is an important component of evolutionary divergence and speciation. Divergence by sexual selection is implicated in faster rates of divergence of the X chromosome and of genes thought to underlie sexually selected traits, including genes that are sex biased in expression. However, accurately inferring the relative importance of complex and interacting forms of natural selection, demography, and neutral processes that occurred in the evolutionary past is challenging. Experimental evolution provides an opportunity to apply controlled treatments for multiple generations and examine the consequent genomic divergence. Here, we altered sexual selection intensity, elevating sexual selection in polyandrous lines and eliminating it in monogamous lines, and examined patterns of allele frequency divergence in the genome of Drosophila pseudoobscura after more than 160 generations of experimental evolution. Divergence is not uniform across the genome but concentrated in islands, many of which contain candidate genes implicated in mating behaviors and other sexually selected phenotypes. These are more often seen on the X chromosome, which also shows greater divergence in F-ST than neutral expectations. There are characteristic signatures of selection seen in these regions, with lower diversity on the X chromosome than the autosomes, and differences in diversity on the autosomes between selection regimes. Reduced Tajima's D within some of the divergent regions may imply that selective sweeps have occurred, despite considerable recombination. These changes are associated with both differential gene expression between the lines and sex-biased gene expression within the lines. Our results are very similar to those thought to implicate sexual selection in divergence between species and natural populations, and hence provide experimental support for the likely role of sexual selection in driving such types of genetic divergence, but also illustrate how variable outcomes can be for different genomic regions.
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12.
  • Zwoinska, Martyna K., et al. (author)
  • Phenotypic Responses to and Genetic Architecture of Sterility Following Exposure to Sub-Lethal Temperature During Development
  • 2020
  • In: Frontiers in Genetics. - : Frontiers Media SA. - 1664-8021. ; 11
  • Journal article (peer-reviewed)abstract
    • Thermal tolerance range, based on temperatures that result in incapacitating effects, influences species' distributions and has been used to predict species' response to increasing temperature. Reproductive performance may also be negatively affected at less extreme temperatures, but such sublethal heat-induced sterility has been relatively ignored in studies addressing the potential effects of, and ability of species' to respond to, predicted climate warming. The few studies examining the link between increased temperature and reproductive performance typically focus on adults, although effects can vary between life history stages. Here we assessed how sublethal heat stress during development impacted subsequent adult fertility and its plasticity, both of which can provide the raw material for evolutionary responses to increased temperature. We quantified phenotypic and genetic variation in fertility ofDrosophila melanogasterreared at standardized densities in three temperatures (25, 27, and 29 degrees C) from a set of lines of theDrosophilaGenetic Reference Panel (DGRP). We found little phenotypic variation at the two lower temperatures with more variation at the highest temperature and for plasticity. Males were more affected than females. Despite reasonably large broad-sense heritabilities, a genome-wide association study found little evidence for additive genetic variance and no genetic variants were robustly linked with reproductive performance at specific temperatures or for phenotypic plasticity. We compared results on heat-induced male sterility with other DGRP results on relevant fitness traits measured after abiotic stress and found an association between male susceptibility to sterility and male lifespan reduction following oxidative stress. Our results suggest that sublethal stress during development has profound negative consequences on male adult reproduction, but despite phenotypic variation in a population for this response, there is limited evolutionary potential, either through adaptation to a specific developmental temperature or plasticity in response to developmental heat-induced sterility.
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13.
  • Barata, Carolina, et al. (author)
  • Selection on the Fly : Short-Term Adaptation to an Altered Sexual Selection Regime in Drosophila pseudoobscura
  • 2023
  • In: Genome Biology and Evolution. - 1759-6653. ; 15:7
  • Journal article (peer-reviewed)abstract
    • Experimental evolution studies are powerful approaches to examine the evolutionary history of lab populations. Such studies have shed light on how selection changes phenotypes and genotypes. Most of these studies have not examined the time course of adaptation under sexual selection manipulation, by resequencing the populations' genomes at multiple time points. Here, we analyze allele frequency trajectories in Drosophila pseudoobscura where we altered their sexual selection regime for 200 generations and sequenced pooled populations at 5 time points. The intensity of sexual selection was either relaxed in monogamous populations (M) or elevated in polyandrous lines (E). We present a comprehensive study of how selection alters population genetics parameters at the chromosome and gene level. We investigate differences in the effective population size-N-e-between the treatments, and perform a genome-wide scan to identify signatures of selection from the time-series data. We found genomic signatures of adaptation to both regimes in D. pseudoobscura. There are more significant variants in E lines as expected from stronger sexual selection. However, we found that the response on the X chromosome was substantial in both treatments, more pronounced in E and restricted to the more recently sex-linked chromosome arm XR in M. In the first generations of experimental evolution, we estimate N-e to be lower on the X in E lines, which might indicate a swift adaptive response at the onset of selection. Additionally, the third chromosome was affected by elevated polyandry whereby its distal end harbors a region showing a strong signal of adaptive evolution especially in E lines.
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14.
  • Baur, Julian, et al. (author)
  • Evolution under increased male postcopulatory sexual selection reduces fertility under heat stress
  • Other publication (other academic/artistic)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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15.
  • Baur, Julian, et al. (author)
  • Heat stress reveals a fertility debt owing to postcopulatory sexual selection
  • 2023
  • In: Evolution Letters. - : Oxford University Press (OUP). - 2056-3744. ; 8:1, s. 101-113
  • Journal article (peer-reviewed)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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16.
  • Baur, Julian, et al. (author)
  • Heat stress reveals a fertility debt owing to postcopulatory sexual selection
  • 2024
  • In: Evolution Letters. - : Oxford University Press. - 2056-3744. ; 8:1, s. 101-113
  • Journal article (peer-reviewed)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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17.
  • Fitzpatrick, John L., et al. (author)
  • Repeated evidence that the accelerated evolution of sperm is associated with their fertilization function
  • 2020
  • In: Proceedings of the Royal Society of London. Biological Sciences. - : The Royal Society. - 0962-8452 .- 1471-2954. ; 287:1932
  • Journal article (peer-reviewed)abstract
    • Spermatozoa are the most morphologically diverse cell type, leading to the widespread assumption that they evolve rapidly. However, there is no direct evidence that sperm evolve faster than other male traits. Such a test requires comparing male traits that operate in the same selective environment, ideally produced from the same tissue, yet vary in function. Here, we examine rates of phenotypic evolution in sperm morphology using two insect groups where males produce fertile and non-fertile sperm types (Drosophila species from the obscura group and a subset of Lepidoptera species), where these constraints are solved. Moreover, in Drosophila we test the relationship between rates of sperm evolution and the link with the putative selective pressures of fertilization function and postcopulatory sexual selection exerted by female reproductive organs. We find repeated evolutionary patterns across these insect groups-lengths of fertile sperm evolve faster than non-fertile sperm. In Drosophila, fertile sperm length evolved faster than body size, but at the same rate as female reproductive organ length. We also compare rates of evolution of different sperm components, showing that head length evolves faster in fertile sperm while flagellum length evolves faster in non-fertile sperm. Our study provides direct evidence that sperm length evolves more rapidly in fertile sperm, probably because of their functional role in securing male fertility and in response to selection imposed by female reproductive organs.
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18.
  • Fitzpatrick, John, et al. (author)
  • SpermTree, a species-level database of sperm morphology spanning the animal tree of life
  • 2022
  • In: Scientific Data. - : Springer Science and Business Media LLC. - 2052-4463. ; 9:1
  • Journal article (peer-reviewed)abstract
    • Sperm are the most morphologically variable cell type known, despite performing the same functional role of fertilizing eggs across all sexually reproducing species. Sperm morphology commonly varies among individuals, populations, closely related species, and across animal phyla. Sperm morphology has long been used as a tool for placing species in a phylogenetic context and a range of selective forces are hypothesized to influence sperm evolution and diversification. However, we currently lack robust examinations of macroevolutionary (i.e. across phyla) patterns of sperm evolution, due largely to the challenges of comparing sperm morphological data across the animal tree of life. Here we describe the SpermTree database, which currently represents 5,675 morphological descriptions of sperm morphology from 4,705 unique species from 27 animal phyla. This dataset includes measurements of sperm head, midpiece, flagellum and total length, the latter of which spans four orders of magnitude. All entries in the dataset are matched to currently accepted scientific names in taxonomic databases, facilitating the use of these data in analyses examining sperm evolution in animals.
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19.
  • Garlovsky, Martin D., et al. (author)
  • Experimental sexual selection affects the evolution of physiological and life-history traits
  • 2022
  • In: Journal of Evolutionary Biology. - : Wiley. - 1010-061X .- 1420-9101. ; 35:5, s. 742-751
  • Journal article (peer-reviewed)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. 
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20.
  • Garlovsky, Martin D., et al. (author)
  • Persistent postmating, prezygotic reproductive isolation between populations
  • 2018
  • In: Ecology and Evolution. - : Wiley. - 2045-7758. ; 8:17, s. 9062-9073
  • Journal article (peer-reviewed)abstract
    • Studying reproductive barriers between populations of the same species is critical to understand how speciation may proceed. Growing evidence suggests postmating, prezygotic (PMPZ) reproductive barriers play an important role in the evolution of early taxonomic divergence. However, the contribution of PMPZ isolation to speciation is typically studied between species in which barriers that maintain isolation may not be those that contributed to reduced gene flow between populations. Moreover, in internally fertilizing animals, PMPZ isolation is related to male ejaculatefemale reproductive tract incompatibilities but few studies have examined how mating history of the sexes can affect the strength of PMPZ isolation and the extent to which PMPZ isolation is repeatable or restricted to particular interacting genotypes. We addressed these outstanding questions using multiple populations of Drosophila montana. We show a recurrent pattern of PMPZ isolation, with flies from one population exhibiting reproductive incompatibility in crosses with all three other populations, while those three populations were fully fertile with each other. Reproductive incompatibility is due to lack of fertilization and is asymmetrical, affecting female fitness more than males. There was no effect of male or female mating history on reproductive incompatibility, indicating that PMPZ isolation persists between populations. We found no evidence of variability in fertilization outcomes attributable to different femalexmale genotype interactions, and in combination with our other results, suggests that PMPZ isolation is not driven by idiosyncratic genotypexgenotype interactions. Our results show PMPZ isolation as a strong, consistent barrier to gene flow early during speciation and suggest several targets of selection known to affect ejaculate-female reproductive tract interactions within species that may cause this PMPZ isolation.
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21.
  • Garlovsky, Martin D., et al. (author)
  • Seminal fluid protein divergence among populations exhibiting postmating prezygotic reproductive isolation
  • 2020
  • In: Molecular Ecology. - : Wiley. - 0962-1083 .- 1365-294X. ; 29:22, s. 4428-4441
  • Journal article (peer-reviewed)abstract
    • Despite holding a central role in fertilization, reproductive traits often show elevated rates of evolution and diversification. The rapid evolution of seminal fluid proteins (Sfps) within populations is predicted to cause mis-signalling between the male ejaculate and the female during and after mating resulting in postmating prezygotic (PMPZ) isolation between populations. Crosses betweenDrosophila montanapopulations show PMPZ isolation in the form of reduced fertilization success in both noncompetitive and competitive contexts. Here we test whether male ejaculate proteins produced in the accessory glands or ejaculatory bulb differ between populations using liquid chromatography tandem mass spectrometry. We find more than 150 differentially abundant proteins between populations that may contribute to PMPZ isolation, including a number of proteases, peptidases and several orthologues ofDrosophila melanogasterSfps known to mediate fertilization success. Males from the population that elicit the stronger PMPZ isolation after mating with foreign females typically produced greater quantities of Sfps. The accessory glands and ejaculatory bulb show enrichment for different gene ontology (GO) terms and the ejaculatory bulb contributes more differentially abundant proteins. Proteins with a predicted secretory signal evolve faster than nonsecretory proteins. Finally, we take advantage of quantitative proteomics data for threeDrosophilaspecies to determine shared and unique GO enrichments of Sfps between taxa and which potentially mediate PMPZ isolation. Our study provides the first high-throughput quantitative proteomic evidence showing divergence of reproductive proteins between populations that exhibit PMPZ isolation.
  •  
22.
  • Garlovsky, Martin D., et al. (author)
  • Within-population sperm competition intensity does not predict asymmetry in conpopulation sperm precedence
  • 2020
  • In: Philosophical Transactions of the Royal Society of London. Biological Sciences. - : The Royal Society. - 0962-8436 .- 1471-2970. ; 375:1813
  • Journal article (peer-reviewed)abstract
    • Postcopulatory sexual selection can generate evolutionary arms races between the sexes resulting in the rapid coevolution of reproductive phenotypes. As traits affecting fertilization success diverge between populations, postmating prezygotic (PMPZ) barriers to gene flow may evolve. Conspecific sperm precedence is a form of PMPZ isolation thought to evolve early during speciation yet has mostly been studied between species. Here, we show conpopulation sperm precedence (CpSP) between Drosophila montana populations. Using Pool-seq genomic data we estimate divergence times and ask whether PMPZ isolation evolved in the face of gene flow. We find models incorporating gene flow fit the data best indicating populations experienced considerable gene flow during divergence. We find CpSP is asymmetric and mirrors asymmetry in non-competitive PMPZ isolation, suggesting these phenomena have a shared mechanism. However, we show asymmetry is unrelated to the strength of postcopulatory sexual selection acting within populations. We tested whether overlapping foreign and coevolved ejaculates within the female reproductive tract altered fertilization success but found no effect. Our results show that neither time since divergence nor sperm competitiveness predicts the strength of PMPZ isolation. We suggest that instead cryptic female choice or mutation-order divergence may drive divergence of postcopulatory phenotypes resulting in PMPZ isolation. This article is part of the theme issue 'Fifty years of sperm competition'.
  •  
23.
  • Immonen, Elina, et al. (author)
  • Mating system variation drives rapid evolution of the female transcriptome in Drosophila pseudoobscura
  • 2014
  • In: Ecology and Evolution. - : Wiley. - 2045-7758. ; 4:11, s. 2186-2201
  • Journal article (peer-reviewed)abstract
    • Interactions between the sexes are believed to be a potent source of selection on sex-specific evolution. The way in which sexual interactions influence male investment is much studied, but effects on females are more poorly understood. To address this deficiency, we examined gene expression in virgin female Drosophila pseudoobscura following 100 generations of mating system manipulations in which we either elevated polyandry or enforced monandry. Gene expression evolution following mating system manipulation resulted in 14% of the transcriptome of virgin females being altered. Polyandrous females elevated expression of a greater number of genes normally enriched in ovaries and associated with mitosis and meiosis, which might reflect female investment into reproductive functions. Monandrous females showed a greater number of genes normally enriched for expression in somatic tissues, including the head and gut and associated with visual perception and metabolism, respectively. By comparing our data with a previous study of sex differences in gene expression in this species, we found that the majority of the genes that are differentially expressed between females of the selection treatments show female-biased expression in the wild-type population. A striking exception is genes associated with male-specific reproductive tissues (in D.melanogaster), which are upregulated in polyandrous females. Our results provide experimental evidence for a role of sex-specific selection arising from differing sexual interactions with males in promoting rapid evolution of the female transcriptome.
  •  
24.
  • Kahrl, Ariel F., et al. (author)
  • Fertilization mode differentially impacts the evolution of vertebrate sperm components
  • 2022
  • In: Nature Communications. - : Springer Science and Business Media LLC. - 2041-1723. ; 13
  • Journal article (peer-reviewed)abstract
    • Environmental change frequently drives morphological diversification, including at the cellular level. Transitions in the environment where fertilization occurs (i.e., fertilization mode) are hypothesized to be a driver of the extreme diversity in sperm morphology observed in animals. Yet how fertilization mode impacts the evolution of sperm components—head, midpiece, and flagellum—each with different functional roles that must act as an integrated unit remains unclear. Here, we test this hypothesis by examining the evolution of sperm component lengths across 1103 species of vertebrates varying in fertilization mode (external vs. internal fertilization). Sperm component length is explained in part by fertilization mode across vertebrates, but how fertilization mode influences sperm evolution varies among sperm components and vertebrate clades. We also identify evolutionary responses not influenced by fertilization mode: midpieces evolve rapidly in both external and internal fertilizers. Fertilization mode thus influences vertebrate sperm evolution through complex component- and clade-specific evolutionary responses.
  •  
25.
  • Kahrl, Ariel F., et al. (author)
  • Fertilization mode drives sperm length evolution across the animal tree of life
  • 2021
  • In: Nature Ecology & Evolution. - : Springer Science and Business Media LLC. - 2397-334X. ; 5:8, s. 1153-1164
  • Journal article (peer-reviewed)abstract
    • Evolutionary biologists have endeavoured to explain the extraordinary diversity of sperm morphology across animals for more than a century. One hypothesis to explain sperm diversity is that sperm length is shaped by the environment where fertilization takes place (that is, fertilization mode). Evolutionary transitions in fertilization modes may transform how selection acts on sperm length, probably by affecting postcopulatory mechanisms of sperm competition and the scope for cryptic female choice. Here, we address this hypothesis by generating a macro-evolutionary view of how fertilization mode (including external fertilizers, internal fertilizers and spermcasters) influences sperm length diversification among 3,233 species from 21 animal phyla. We show that sperm are shorter in species whose sperm are diluted in aquatic environments (that is, external fertilizers and spermcasters) and longer in species where sperm are directly transferred to females (that is, internal fertilizers). We also show that sperm length evolves faster and with a greater number of adaptive shifts in species where sperm operate within females (for example, spermcasters and internal fertilizers). Our results demonstrate that fertilization mode is a key driver in the evolution of sperm length across animals, and we argue that a complex combination of postcopulatory forces has shaped sperm length diversification throughout animal evolution.
  •  
26.
  • Karr, Timothy L., et al. (author)
  • The Old and the New : Discovery Proteomics Identifies Putative Novel Seminal Fluid Proteins in Drosophila
  • 2019
  • In: Molecular & Cellular Proteomics. - 1535-9476 .- 1535-9484. ; 18:3, s. S23-S33
  • Journal article (peer-reviewed)abstract
    • Seminal fluid proteins (SFPs), the nonsperm component of male ejaculates produced by male accessory glands, are viewed as central mediators of reproductive fitness. SFPs effect both male and female post-mating functions and show molecular signatures of rapid adaptive evolution. Although Drosophila melanogaster is the dominant insect model for understanding SFP evolution, understanding of SFP evolutionary causes and consequences require additional comparative analyses of close and distantly related taxa. Although SFP identification was historically challenging, advances in label-free quantitative proteomics expands the scope of studying other systems to further advance the field. Focused studies of SFPs has so far overlooked the proteomes of male reproductive glands and their inherent complex protein networks for which there is little information on the overall signals of molecular evolution. Here we applied label-free quantitative proteomics to identify the accessory gland proteome and secretome in Drosophila pseudoobscura, a close relative of D. melanogaster, and use the dataset to identify both known and putative novel SFPs. Using this approach, we identified 163 putative SFPs, 32% of which overlapped with previously identified D. melanogaster SFPs and show that SFPs with known extracellular annotation evolve more rapidly than other proteins produced by or contained within the accessory gland. Our results will further the understanding of the evolution of SFPs and the underlying male accessory gland proteins that mediate reproductive fitness of the sexes.
  •  
27.
  • Macartney, Erin, et al. (author)
  • Intra-specific correlations between ejaculate traits and competitive fertilization success : a meta-analysis across species and fertilization modes
  • 2023
  • In: Evolution. - 0014-3820 .- 1558-5646. ; 78:3, s. 497-510
  • Journal article (peer-reviewed)abstract
    • Understanding of how selection can act on traits that improve competitiveness and subsequent paternity has advanced, including the idea that internal and external fertilization presents different environments that may select differentially on ejaculate traits. However, no studies have quantitatively synthesized the intra-specific relationships between these traits and paternity. Therefore, we conducted a meta-analysis across 52 papers to determine which ejaculate traits positively correlate with paternity share and how these correlations vary with fertilization mode. Overall, most ejaculate traits were positively associated with paternity, with the notable exception of sperm length. Sub-analyses on sperm number, sperm length, and sperm velocity revealed no statistical differences between fertilization modes in the relationship between traits and paternity when all effect sizes across species were combined. However, in a sub-analysis on fish species only, we found evidence that sperm velocity may be more important in external fertilizers. We also observed differences in the importance of phylogenetic relatedness and some species-specific differences. Our results suggest that while most ejaculate traits should be under positive directional selection in both internal and external fertilizers, sperm length may be subject to more nuanced selection pressures. Overall, we highlight important patterns of intra-specific relationships between ejaculate traits and competitive fertilization success.
  •  
28.
  • Poikela, Noora, et al. (author)
  • Strength of sexual and postmating prezygotic barriers varies between sympatric populations with different histories and species abundances
  • 2019
  • In: Evolution. - : Wiley. - 0014-3820 .- 1558-5646. ; 73:6, s. 1182-1199
  • Journal article (peer-reviewed)abstract
    • The impact of different reproductive barriers on species or population isolation may vary in different stages of speciation depending on evolutionary forces acting within species and through species' interactions. Genetic incompatibilities between interacting species are expected to reinforce prezygotic barriers in sympatric populations and lead to cascade reinforcement between conspecific populations living within and outside the areas of sympatry. We tested these predictions and studied whether and how the strength and target of reinforcement between Drosophila montana and Drosophila flavomontana vary between sympatric populations with different histories and species abundances. All barriers between D. montana females and D. flavomontana males were nearly complete, while in the reciprocal cross strong postzygotic isolation was accompanied by prezygotic barriers whose strength varied according to population composition. Sexual isolation between D. flavomontana females and D. montana males was increased in long-established sympatric populations, where D. flavomontana is abundant, while postmating prezygotic (PMPZ) barriers were stronger in populations where this species is a new invader and still rare and where female discrimination against heterospecific males was lower. Strengthening of sexual and PMPZ barriers in this cross also induced cascade reinforcement of respective barriers between D. flavomontana populations, which is a classic signature of reinforcement process.
  •  
29.
  • Rohner, Patrick T., et al. (author)
  • Interrelations of global macroecological patterns in wing and thorax size, sexual size dimorphism, and range size of the Drosophilidae
  • 2018
  • In: Ecography. - : Wiley. - 0906-7590 .- 1600-0587. ; 41:10, s. 1707-1717
  • Journal article (peer-reviewed)abstract
    • Support for macroecological rules in insects is mixed, with potential confounding interrelations between patterns rarely studied. We here investigate global patterns in body and wing size, sexual size dimorphism and range size in common fruit flies (Diptera: Drosophilidae) and explore potential interrelations and the predictive power of Allen's, Bergmann's, Rensch's and Rapoport's rules. We found that thorax length (r2 = 0.05) and wing size (r2 = 0.09) increased with latitude, supporting Bergmann's rule. Contrary to patterns often found in endothermic vertebrates, relative wing size increased towards the poles (r2 = 0.12), a pattern against Allen's rule, which we attribute to selection for increased flight capacity in the cold. Sexual size dimorphism decreased with size, evincing Rensch's rule across the family (r2 = 0.14). Yet, this pattern was largely driven by the virilis–repleta radiation. Finally, range size did not correlate with latitude, although a positive relationship was present in a subset of the species investigated, providing no convincing evidence for Rapoport's rule. We further found little support for confounding interrelations between body size, wing loading and range size in this taxon. Nevertheless, we demonstrate that studying several traits simultaneously at minimum permits better interpretation in case of multiple, potentially conflicting trends or hypotheses concerning the macroecology of insects.
  •  
30.
  • Southern, Helen M., et al. (author)
  • Sperm morphology and the evolution of intracellular sperm-egg interactions
  • 2018
  • In: Ecology and Evolution. - : Wiley. - 2045-7758. ; 8:10, s. 5047-5058
  • Journal article (peer-reviewed)abstract
    • Sperm morphology is incredibly diverse, even among closely related species, yet the coevolution between males and females of fertilization recognition systems is necessary for successful karyogamy (male and female pronuclear fusion). In most species, the entire sperm enters the egg during fertilization so sperm morphological diversity may impact the intracellular sperm-egg interactions necessary for karyogamy. We quantified morphological variation of sperm inside eggs prior to and following karyogamy in several species of Drosophila to understand whether evolution of sperm morphology could influence intracellular sperm-egg interactions (ISEIs). We measured seven parameters that describe ISEIs among species to determine whether these parameters varied both within a species across development and across species at the same developmental stage. We used heterospecific crosses to test the relative role of male origin, female origin, and interaction between the male and female in determining ISEIs. We found that sperm shape changed within a species as development proceeded and, at particular development stages, species varied in some ISEIs. Parental origin had an effect on some ISEIs, with a general trend for a stronger female effect. Overall, our findings identify conserved and variable ISEIs among species and demonstrate the potential to contribute understanding to gamete evolution and development.
  •  
31.
  • Tunström, Kalle, 1991- (author)
  • Understanding evolutionary novelty through female-limited polymorphisms
  • 2023
  • Doctoral thesis (other academic/artistic)abstract
    • Understanding how novel traits evolve is a central question in evolutionary biology. However, unraveling the complex genetic and developmental mechanisms underlying trait innovation can be challenging, especially when the trait evolved a long time ago. One approach to this complexity is to leverage natural polymorphisms, revealing variation in the expression or function of novel traits. Polymorphisms can provide insights into the origin, maintenance, and diversification of trait innovation, and the evolutionary forces and constraints shaping them. Sex-limited polymorphisms, a special class of polymorphism in which only one sex exhibits variation in the trait, can be particularly informative because they allow for the investigation of not only the genetic basis and evolutionary history of novel traits, but also how differences between sexes (sexual dimorphisms) are regulated and evolve.In my thesis, I utilize naturally occurring female-limited color polymorphisms to answer questions about the evolutionary origin, mechanism, and maintenance of wing coloration and patterning variation in butterflies.  Butterfly wing coloration and patterning are not only striking examples of morphological diversity but also critical to survival and fitness. While butterfly wing patterning and coloration have inspired evolutionary thinking  for over a century, they have recently become a model system for Evo-Devo research. As easily visually assessed traits, butterfly wings have proven perfect candidates for more recent advances in Evo-Devo, acting as a template for understanding the function, recruitment, and evolution of gene regulatory networks (GRNs) generating complex phenotypes. In Paper I, I reconstruct the evolutionary history of Alba, a genetically determined female-limited alternative life history strategy, found in over one third of species in the genus Colias (Pieridae). In this polymorphism, some Colias females redirect resources from wing coloration to reproductive development, resulting in white rather than orange wings. I show this polymorphism evolved once in the Colias phylogeny through a transposable element insertion and has persisted for over a million years through balancing selection and introgression. In Paper II, I dissect the pteridine biosynthesis pathway, a pigment that Pierid butterflies, including Colias, use to color their wings. I highlight not only the extent of pteridine use by Pierid butterflies, but also evidence suggesting novel evolution for core components of the biosynthesis pathway. In Paper III, I investigate the genetic basis of a regionally isolated sexual dimorphism in Pieris napi, called adalvinda. Rather than the creamy white wings seen in the rest of the range, females in northern Scandinavian populations have highly melanized, almost dark brown wings. Similarly to Paper I, I in Paper III identify a transposable element insertion, but this time upstream of the gene cortex associated with female wing melanization. This finding contributes to a growing body of literature linking cortex with butterfly wing melanization, while emphasizing the potential role transposable elements may play in the evolution of novel – and especially female-limited or sexually dimorphic – traits. Lastly, in Paper IV, I present a new reference genome for the Edith's Checkerspot butterfly, offering an important resource for future functional genomic and conservation analyses, and demonstrating an efficient framework for developing genetic resources for non-model systems. In summary, my thesis demonstrates the powerful potential of utilizing naturally occurring polymorphisms or induced mutations to study the evolution of novel traits.
  •  
32.
  • Urban, Mark C., et al. (author)
  • When and how can we predict adaptive responses to climate change?
  • 2024
  • In: Evolution Letters. - : Oxford University Press. - 2056-3744. ; 8:1, s. 172-187
  • Journal article (peer-reviewed)abstract
    • Predicting if, when, and how populations can adapt to climate change constitutes one of the greatest challenges in science today. Here, we build from contributions to the special issue on evolutionary adaptation to climate change, a survey of its authors, and recent literature to explore the limits and opportunities for predicting adaptive responses to climate change. We outline what might be predictable now, in the future, and perhaps never even with our best efforts. More accurate predictions are expected for traits characterized by a well-understood mapping between genotypes and phenotypes and traits experiencing strong, direct selection due to climate change. A meta-analysis revealed an overall moderate trait heritability and evolvability in studies performed under future climate conditions but indicated no significant change between current and future climate conditions, suggesting neither more nor less genetic variation for adapting to future climates. Predicting population persistence and evolutionary rescue remains uncertain, especially for the many species without sufficient ecological data. Still, when polled, authors contributing to this special issue were relatively optimistic about our ability to predict future evolutionary responses to climate change. Predictions will improve as we expand efforts to understand diverse organisms, their ecology, and their adaptive potential. Advancements in functional genomic resources, especially their extension to non-model species and the union of evolutionary experiments and "omics," should also enhance predictions. Although predicting evolutionary responses to climate change remains challenging, even small advances will reduce the substantial uncertainties surrounding future evolutionary responses to climate change. Preventing biological impacts from climate change will require accurate predictions about which species and ecosystems are most at risk and how best to protect them. Despite some progress, most predictive efforts still omit the potential for evolution to mediate climate change impacts. Here, we evaluate what is predictable now, in the future, and likely never based on recent literature, a survey of authors, and authors' contributions to a special issue on climate change evolution. Evidence indicates a growing ability to predict at least some components underlying evolutionary dynamics. For instance, the direct effects of climate change often alter natural selection regimes that could elicit evolutionary responses assuming sufficient additive genetic variation. We found no evidence for an increase or decrease in evolvability under future climate conditions, but we did find an overall moderate level of evolvability. However, the specific genetics underlying potential adaptive changes are still a "black box" that remains difficult to predict. We not only discuss the opportunities afforded by new genomic techniques to elucidate these genetic black boxes but also caution that the costs and limitations of such techniques for many species might not warrant their general practicality. We highlight further progress and challenges in predicting gene flow and population persistence, both of which can facilitate evolutionary rescue. We finish by listing ten activities that are needed to accelerate future progress in predicting climate change evolution. Despite the many complexities, we are relatively optimistic that evolutionary responses to climate change are becoming more accurate through time, especially assuming a more focused effort to fill key knowledge gaps in the coming years.
  •  
33.
  • White, N. J., et al. (author)
  • Experimental evolution of local adaptation under unidimensional and multidimensional selection
  • 2022
  • In: Current Biology. - : Elsevier BV. - 0960-9822 .- 1879-0445. ; 32:6
  • Journal article (peer-reviewed)abstract
    • Local adaptation is a fundamental evolutionary process generating biological diversity and potentially enabling ecological speciation. Divergent selection underlies the evolution of local adaptation in spatially structured populations by driving their adaptation toward local optima. Environments rarely differ along just one environmental axis; therefore, divergent selection may often be multidimensional. How the dimensionality of divergent selection affects local adaptation is unclear: evolutionary theory predicts that increasing dimensionality will increase local adaptation when associated with stronger overall selection but may have less predictable effects if selection strengths are equal. Experiments are required that allow the effect of the dimensionality of selection on local adaptation to be tested independently of the total strength of selection. We experimentally evolved 32 pairs of monogonont rotifer populations under either unidimensional divergent selection (a single pair of stressors) or multidimensional divergent selection (three pairs of stressors), keeping the total strength of selection equal between treatments. At regular intervals, we assayed fitness in home and away environments to assess local adaptation. We observed an initial increase and subsequent decline of local adaptation in populations exposed to multidimensional selection, compared with a slower but eventually stronger increase in local adaptation in populations exposed to unidimensional selection. Our results contrast with existing predictions, such as the "weak multifarious"and "stronger selection"hypotheses. Instead, we hypothesize that adaptation to multidimensional divergent selection may favor generalist genotypes and only produce transient local adaptation.
  •  
34.
  • White, Nathan J., et al. (author)
  • The Past and Future of Experimental Speciation
  • 2020
  • In: Trends in Ecology & Evolution. - : Elsevier BV. - 0169-5347 .- 1872-8383. ; 35:1, s. 10-21
  • Research review (peer-reviewed)abstract
    • Speciation is the result of evolutionary processes that generate barriers to gene flow between populations, facilitating reproductive isolation. Speciation is typically studied via theoretical models and snapshot tests in natural populations. Experimental speciation enables real-time direct tests of speciation theory and has been long touted as a critical complement to other approaches. We argue that, despite its promise to elucidate the evolution of reproductive isolation, experimental speciation has been underutilised and lags behind other contributions to speciation research. We review recent experiments and outline a framework for how experimental speciation can be implemented to address current outstanding questions that are otherwise challenging to answer. Greater uptake of this approach is necessary to rapidly advance understanding of speciation.
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