Added: Sarahbeth Leo - Date: 16.02.2022 21:28 - Views: 15150 - Clicks: 6681
Researchers have greatly clarified the ways that organisms evolve to improve their survival in warmer climates, yet a major gap in our knowledge remains. Here, we show that mating-related traits in male but not female dragonflies evolve in a highly predictable way as they adapt to climatic conditions.
Failing to for adaptive evolution of mating-related traits may therefore limit our ability to forecast how organisms will respond to climate change. Adaptation to different climates fuels the origins and maintenance of biodiversity. Detailing how organisms optimize fitness for their local climates is therefore an essential goal in biology. Although we increasingly understand how survival-related traits evolve as organisms adapt to climatic conditions, it is unclear whether organisms also optimize traits that coordinate mating between the sexes.
Here, we show that dragonflies consistently adapt to warmer climates across space and time by evolving less male melanin ornamentation—a mating-related trait that also absorbs solar radiation and heats individuals above ambient temperatures. Continent-wide macroevolutionary analyses reveal that species inhabiting warmer climates evolve less male ornamentation.
Observations from to detail that contemporary selective pressures oppose male ornaments in warmer years; and our climate-warming projections predict further decreases by Conversely, our analyses show that female ornamentation responds idiosyncratically to temperature across space and time, indicating the sexes evolve in different ways to meet the demands of the local climate. Overall, these macro- and microevolutionary findings demonstrate that organisms predictably optimize their mating-related traits for the climate just as they do their survival-related traits.
Characterizing how organisms respond to climatic factors, like temperature, is therefore an enduring goal in biology, which has become even more crucial due to the ongoing climate crisis 3. To date, researchers have uncovered many ways that organisms improve survival in their local climates through the evolution of traits such as physiological tolerance 4life cycle timing 5and body size 6. However, recent work reveals that climatic adaptation can also involve optimizing mating and reproduction in addition to survival 7.
The evolution of sexual traits that coordinate mating could therefore be an important way that plants and animals improve fitness in their local climate from one generation to the next. One type of sexual trait that could often be involved in climatic adaptation is ornamental coloration, which many animals use to attract mates and intimidate rivals. Alternatively, because tropical species are frequently more ornately colored than their temperate relatives, some researchers have suggested that adaptation to warmer climates may instead favor more exaggerated ornamentation By understanding how ornamental coloration responds to selective pressures in different climates, we can begin to resolve if the evolution of sexual traits is indeed a major feature of how organisms adapt to the climate 3 If, for example, selective pressures in warmer climates require the evolution of less exaggerated ornamentation, then we should observe that animals inhabiting hotter environments consistently evolve less ornamental color regardless of timescale or historical contingencies e.
Dragonflies and damselflies are well suited for such tests because they possess ornamental wing melanization that varies within and among species Such heating may provide modest locomotor benefits under cool conditions 11but it can damage wing tissue, reduce male fighting ability and territorial Woman sex contact Seehausen, and even cause death under warm conditions 11 These sex-specific thermal consequences for both reproduction and survival suggest that dragonflies should adapt to their local climates across space and time through the evolution of ornamental wing melanization in males but not necessarily in females 11 We tested this hypothesis by exploring how male and female ornaments have responded to climatic differences across the macroevolutionary, microevolutionary, and contemporary history of Nearctic dragonflies.
To first evaluate if selective pressures in different climates have favored ornament evolution across macroevolutionary Woman sex contact Seehausen, we tested if Nearctic dragonfly species inhabiting warmer ranges are less likely to have evolved wing melanization than those inhabiting cooler ranges. After controlling for shared evolutionary history, we found sex-specific patterns of ornament evolution among climates. However, interspecific patterns for female wing melanization contrasted starkly with these patterns for males. Thus, the evolution of male, but not female, wing melanization is a component of how dragonflies respond to climatic differences over long timescales.
Macroevolution of dragonfly wing melanization in relation to temperature. A Nearctic dragonfly phylogeny. Filled tips indicate the presence of male green and female purple wing melanization. B Dragonfly species across the Nearctic. C and D Probability of males C and females D possessing wing melanization. These macroevolutionary findings indicate that selective pressures in warmer climates have favored less male, but not female, ornamentation among Nearctic dragonfly species.
However, most dragonfly species are much older than their current geographic distributions Thus, as is true in many studies of ancient lineages, these biogeographic patterns probably stem from both ecological filtering and adaptation. For instance, following the Last Glacial Maximum, species may have Woman sex contact Seehausen regions where the climatic conditions did not make male ornamentation too costly i.
Additionally, because ornamentation is quite evolutionarily labile 18these macroevolutionary patterns likely also arise from adaptation to local climates. The relative contributions of colonization and adaptation to interspecific ornament variation cannot yet be disentangled for this group or for many other ancient clades. Nevertheless, if adaptation to local climatic conditions has led species to evolve differing ornamentation over long timescales, then it should also entail ornament evolution across shorter timescales—such as those separating populations within the same species.
To evaluate if populations consistently adapt to their local climates via ornament evolution, we next tested for parallel shifts in ornament size across the ranges of 10 widely distributed Nearctic dragonfly species 14 Fig. Within 7 of the 10 species, males in warmer regions had ificantly less wing melanization than their counterparts in cooler areas Fig. Because developing at warmer temperatures does not induce male dragonflies to express less ornamentation 20genetic differences among populations are more likely to underlie these parallel responses than phenotypic plasticity alone.
In contrast to the patterns in males, females possessed ificantly less wing melanization in warmer climates for only 3 out of 10 species Fig. Thus, mirroring macroevolutionary patterns among species, the differing selective pressures among climates also favor consistent patterns of sex-specific ornament evolution within species Fig. In particular, these sex-specific responses within species result in male ornaments being Parallel evolution of wing melanization in response to mean annual temperature MAT within dragonfly species.
Asterisks indicate ificant declines. The ornament evolution that ly facilitated adaptation over thousands of years may therefore need to occur over fewer than generations unless alternative responses can be employed. For instance, more-ornamented species could lessen the threat of overheating by tracking northward shifts of cooler temperatures.
More-ornamented species could also alleviate the risk of overheating by shifting phenology to defend territories in cooler times of day or to reproduce in cooler times of year To evaluate how natural and sexual selection might alter ornamentation as the Earth warms, we tested if the 10 widely distributed dragonfly species Fig. However, since males and females responded more similarly to each other across annual variation than geographic variation, the estimated extent of sexual dimorphism was only modestly more male biased in cold years The temporal patterns in ornament size therefore likely emerge from processes operating within generations rather than across generations.
As dragonflies do not develop less wing melanization when reared under warmer conditions 20a probable explanation for this within-generation effect is that selection in warmer years consistently reduces the of highly ornamented individuals in breeding Woman sex contact Seehausen. Wing melanization shifts with interannual temperature variation. Since selective pressures in warmer years appear to favor less ornamented males, we estimated how wing melanization might shift as North America warms over the next several decades. Based on the best- and worst-case scenarios for climatic warming 21we used the current geographic relationship between ornamentation and temperature to forecast the amount of wing melanization each species should possess in for the coolest third, thermal midpoint, and warmest third of its range 2124 SI AppendixTable S3.
Assuming that phenotypic selection underlies the interannual ornament variation we observed Fig. For male ornamentation to keep pace with this intensity of selection each generation, heritability would need to average 0. Because the capacity for rapid responses to climatic warming is often limited along other phenotypic axes [e.
Collectively, our analyses indicate that male, but not female, ornament evolution is a predictable feature of climatic adaptation in dragonflies. Males experience different thermal conditions from females primarily while defending sunlit territories, and selection in this reproductive context therefore seems likely to underlie the male-specific patterns of divergence.
However, studying how male ornaments tly affect survival, territorial success, and courtship success in warm versus cool regions will Woman sex contact Seehausen necessary to identify which selective mechanisms are directly responsible for the parallel patterns of ornament evolution. Alternatively, the potential advantages of ornament-induced heating for success at fighting rivals or courting mates in cool climates could facilitate male ornament exaggeration in those regions We also cannot rule out that other factors contribute to male ornament evolution among climates.
For instance, highly ornamented males may incur disproportionate metabolic costs in warmer environments if they are challenged more frequently by rivals Regardless of the precise mechanism sour show that climatic adaptation in dragonflies entails some of the most predictable responses ever observed for a sexual trait 8.
In contrast to parallel responses among males, our study reveals that females adapt more idiosyncratically to the climate across space and time. In particular, female ornaments show no consistent relationship with climatic conditions within or among species, suggesting that ornaments have different thermal consequences for males and females However, future research should include investigations of: 1 why females do not take greater advantage of the potential benefits of ornament-induced heating in cool climates, and 2 what other selective pressures shape female ornament evolution [e.
Nevertheless, though we often assume that climatic adaptation requires similar evolution between the sexes 3our findings indicate that the climate should be considered alongside the many other environmental factors for which adaptive evolution is known to be sex specific Our projections further indicate that sex-specific ornament evolution will be a plausible response to future global warming. For species that began the current interglacial period with little sexual dimorphism, selection would have favored male-biased ornamentation during expansion into northern climates Male ornaments may then have less standing genetic variation in northern regions for such taxa, which could greatly constrain the forecasted evolutionary reductions for those populations Table 1.
Alternatively, for species that had considerable sexual dimorphism at the end of the last glaciation, selection in ly unglaciated areas would have favored low levels of ornamentation in both sexes as the planet gradually warmed In this scenario, historical selection in southern populations would have winnowed genetic variation in male ornaments Woman sex contact Seehausen promoted strong between-sex genetic correlations Because the optimal response should differ between the sexes in the coming years Table 1any strong between-sex genetic correlations could impede climatic adaptation for these populations.
Overall, we have shown that climatic adaptation requires optimizing mating-related traits across space and time. Because melanin coloration is a taxonomically widespread character that animals and plants use to coordinate reproduction 934the patterns of ornament evolution that we observed here may be a major feature of climatic adaptation in many organisms. However, the tree of life contains a remarkable array of ornaments, weapons, and vocalizations, and much remains unknown about the breadth of ways that organisms optimize their sexual traits for reproduction in different climates.
Though the direction of evolution may not be the same for every sexual trait or every organism, our findings demonstrate that mating-related traits are a dimension of the phenotype that must be optimized for the local climate just like survival-related traits.
After pruning a recently published odonate phylogeny to the focal species 3940we first used a phylogenetic logistic regression [phylolm 41 ] to assess how climatic temperature influences the likelihood of a species possessing male and female wing melanization.
We fit separate models for each sex. Supplemental analyses revealed precipitation does not underlie the interspecific patterns of ornamentation SI Appendix. were similar when comparing mean range temperature among species with ornaments of differing darkness SI Appendix. We examined ornament variation within 10 species that each possess wing melanization, wide latitudinal ranges, and a large of iNaturalist observations Fig.
For each species, we downloaded Similar approaches have been validated for measuring spatiotemporal variation in animal coloration 19 Using the 2, observations, we tested whether males and females within each species have smaller ornaments in warmer regions. Analogous statistical approaches are common 111945 and provide similar to those that directly incorporate spatial distance among observations Quadratic effects of mean annual temperature were ificant for two species Fig.
To assess if these 10 species were responding in a consistent fashion, we fit a single model for each sex that included the observations of all 10 species as the response and the linear effect of temperature as a fixed effect. Because few species exhibit a quadratic effect of temperature, we considered only the linear effect.
As there was no evidence for phylogenetic al, we did not incorporate a phylogeny into these analyses SI AppendixTable S4 Supplemental analyses indicate that precipitation Woman sex contact Seehausen not underlie the intraspecific patterns of ornamentation SI Appendix. We tested if ornamentation is related to range shifts by updating a dataset of 65 European dragonflies Leveraging iNaturalist observations, we classified if each species possessed wing melanization 11 We then used phylogenetic generalized least squares 48 to test if species with male wing melanization had moved further northward from to than species without it.
As the phylogeny from our main analyses included few of these European species, we employed a digitized version of the phylogeny in their article However, model comparison indicated that the best-supported model did not include phylogeny SI AppendixTable S5 Using the observations in our intraspecific dataset Fig.
We focused on this time period because each sex had at least 15 observations in each of those years.
To ensure any overall relationship between annual temperature and ornamentation was not biased by species-specific responses to geographic variation in temperature Fig. Similar approaches are commonly employed with museum specimens 5051 and have been validated for iNaturalist observations Supplemental analyses indicate that neither temporal nor geographic changes in iNaturalist usage underlie the observed pattern SI Appendix. We further assessed how the extent of sexual dimorphism changed across the focal timespan by estimating the relative size difference in male and female wing melanization in the coolest 0.
We estimated how much wing melanization should Woman sex contact Seehausen in order to track temperatures through For each of the 10 species in our intraspecific dataset, we downloaded forecasted temperatures for the coldest third, thermal midpoint, and the hottest third of their current range To include a realistic range of possible temperatures in each location, we chose the Representative Concentration Pathways RCPs 4. To estimate how each species by sex combination will respond, we calculated the difference between the future and current levels of wing melanization and divided by the SD of the current wing melanization.
Here, the per-generation response to selection was the shift that would be necessary if the Northern Hemisphere warms annually by 0. The intensity of selection for such yearly warming was estimated from the relationship between male wing melanization and mean temperature anomaly Fig. The requisite heritability is then equal to the per-generation response to selection divided by the per-generation intensity of selection.
This work would not have been possible without the thousands of iNaturalist users who photograph dragonflies. Conversations and feedback from C.Woman sex contact Seehausen
email: [email protected] - phone:(763) 681-2626 x 3458
Sex-specific ornament evolution is a consistent feature of climatic adaptation across space and time in dragonflies