Heritable variation in thermal profiles is associated with reproductive success in the world's largest bird.

Organisms inhabiting extreme thermal environments, such as desert birds, have evolved spectacular adaptations to thermoregulate during hot and cold conditions. However, our knowledge of selection for thermoregulation and the potential for evolutionary responses is limited, particularly for large organisms experiencing extreme temperature fluctuations. Here we use thermal imaging to quantify selection and genetic variation in thermoregulation in ostriches (Struthio camelus), the world's largest bird species that is experiencing increasingly volatile temperatures. We found that females who are better at regulating their head temperatures ("thermoregulatory capacity") had higher egg-laying rates under hotter conditions. Thermoregulatory capacity was both heritable and showed signatures of local adaptation: females originating from more unpredictable climates were better at regulating their head temperatures in response to temperature fluctuations. Together these results reveal that past and present evolutionary processes have shaped genetic variation in thermoregulatory capacity, which appears to protect critical organs, such as the brain, from extreme temperatures during reproduction.

The genomics and evolution of inter-sexual mimicry and female-limited polymorphisms in damselflies.

Sex-limited morphs can provide profound insights into the evolution and genomic architecture of complex phenotypes. Inter-sexual mimicry is one particular type of sex-limited polymorphism in which a novel morph resembles the opposite sex. While inter-sexual mimics are known in both sexes and a diverse range of animals, their evolutionary origin is poorly understood. Here, we investigated the genomic basis of female-limited morphs and male mimicry in the common bluetail damselfly. Differential gene expression between morphs has been documented in damselflies, but no causal locus has been previously identified. We found that male mimicry originated in an ancestrally sexually dimorphic lineage in association with multiple structural changes, probably driven by transposable element activity. These changes resulted in ~900 kb of novel genomic content that is partly shared by male mimics in a close relative, indicating that male mimicry is a trans-species polymorphism. More recently, a third morph originated following the translocation of part of the male-mimicry sequence into a genomic position ~3.5 mb apart. We provide evidence of balancing selection maintaining male mimicry, in line with previous field population studies. Our results underscore how structural variants affecting a handful of potentially regulatory genes and morph-specific genes can give rise to novel and complex phenotypic polymorphisms.

Phenotypic selection in natural populations: what have we learned in 40 years?

In 1983, Russell Lande and Stevan Arnold published "The measurement of selection on correlated characters," which became a highly influential citation classic in evolutionary biology. This paper stimulated a cottage industry of field studies of natural and sexual selection in nature and resulted in several large-scale meta-analyses, statistical developments, and method papers. The statistical tools they suggested contributed to a breakdown of the traditional dichotomy between ecological and evolutionary time scales and stimulated later developments such as "eco-evolutionary dynamics". However, regression-based selection analyses also became criticized from philosophical, methodological, and statistical viewpoints and stimulated some still ongoing debates about causality in evolutionary biology. Here I return to this landmark paper by Lande and Arnold, analyze the controversies and debates it gave rise to and discuss the past, present, and future of selection analyses in natural populations. A remaining legacy of Lande & Arnold, 1983 is that studies of selection and inheritance can fruitfully be decoupled and be studied separately, since selection acts on phenotypes regardless of their genetic basis, and hence selection and evolutionary responses to selection are distinct processes.

Evolutionary trade-offs between heat and cold tolerance limit responses to fluctuating climates.

The evolutionary potential of species to cope with short-term temperature fluctuations during reproduction is critical to predicting responses to future climate change. Despite this, vertebrate research has focused on reproduction under high or low temperatures in relatively stable temperate climates. Here, we characterize the genetic basis of reproductive thermal tolerance to temperature fluctuations in the ostrich, which lives in variable environments in tropical and subtropical Africa. Both heat and cold tolerance were under selection and heritable, indicating the potential for evolutionary responses to mean temperature change. However, we found evidence for a negative, genetic correlation between heat and cold tolerance that should limit the potential for adaptation to fluctuating temperatures. Genetic constraints between heat and cold tolerance appear a crucial, yet underappreciated, factor influencing responses to climate change.

Phenotypic plasticity is aligned with phenological adaptation on both micro- and macroevolutionary timescales.

In seasonally variable environments, phenotypic plasticity in phenology may be critical for adaptation to fluctuating environmental conditions. Using an 18-generation longitudinal dataset from natural damselfly populations, we show that phenology has strongly advanced. Individual fitness data suggest this is likely an adaptive response towards a temperature-dependent optimum. A laboratory experiment revealed that developmental plasticity qualitatively matches the temperature dependence of selection, partially explaining observed advance in phenology. Expanding our analysis to the macroevolutionary level, we use a database of over 1-million occurrence records and spatiotemporally matched temperature data from 49 Swedish Odonate species to infer macroevolutionary dynamics of phenology. Phenological plasticity was more closely aligned with adaptation for species that have recently colonised northern latitudes, but with higher phenological mismatch at lower latitudes. Our results show that phenological plasticity plays a key role in microevolutionary dynamics within a single species, and such plasticity may have facilitated post-Pleistocene range expansion in this insect clade.

Latitudinal clines in sexual selection, sexual size dimorphism and sex-specific genetic dispersal during a poleward range expansion.

Range expansions can be shaped by sex differences in behaviours and other phenotypic traits affecting dispersal and reproduction. Here, we investigate sex differences in morphology, behaviour and genomic population differentiation along a climate-mediated range expansion in the common bluetail damselfly (Ischnura elegans) in northern Europe. We sampled 65 sites along a 583-km gradient spanning the I. elegans range in Sweden and quantified latitudinal gradients in site relative abundance, sex ratio and sex-specific shifts in body size and mating status (a measure of sexual selection). Using single nucleotide polymorphism (SNP) data for 426 individuals from 25 sites, we further investigated sex-specific landscape and climatic effects on neutral genetic connectivity and migration patterns. We found evidence for sex differences associated with the I. elegans range expansion, namely (a) increased male body size with latitude, but no latitudinal effect on female body size, resulting in reduced sexual dimorphism towards the range limit, (b) a steeper decline in male genetic similarity with increasing geographic distance than in females, (c) male-biased genetic migration propensity and (d) a latitudinal cline in migration distance (increasing migratory distances towards the range margin), which was stronger in males. Cooler mean annual temperatures towards the range limit were associated with increased resistance to gene flow in both sexes. Sex ratios became increasingly male biased towards the range limit, and there was evidence for a changed sexual selection regime shifting from favouring larger males in the south to favouring smaller males in the north. Our findings suggest sex-specific spatial phenotype sorting at the range limit, where larger males disperse more under higher landscape resistance associated with cooler climates. The combination of latitudinal gradients in sex-biased dispersal, increasing male body size and (reduced) sexual size dimorphism should have emergent consequences for sexual selection dynamics and the mating system at the expanding range front. Our study illustrates the importance of considering sex differences in the study of range expansions driven by ongoing climate change.

The importance of pre- and postcopulatory sexual selection promoting adaptation to increasing temperatures.

Global temperatures are increasing rapidly affecting species globally. Understanding if and how different species can adapt fast enough to keep up with increasing temperatures is of vital importance. One mechanism that can accelerate adaptation and promote evolutionary rescue is sexual selection. Two different mechanisms by which sexual selection can facilitate adaptation are pre- and postcopulatory sexual selection. However, the relative effects of these different forms of sexual selection in promoting adaptation are unknown. Here, we present the results from an experimental study in which we exposed fruit flies Drosophila melanogaster to either no mate choice or 1 of 2 different sexual selection regimes (pre- and postcopulatory sexual selection) for 6 generations, under different thermal regimes. Populations showed evidence of thermal adaptation under precopulatory sexual selection, but this effect was not detected in the postcopulatory sexual selection and the no choice mating regime. We further demonstrate that sexual dimorphism decreased when flies evolved under increasing temperatures, consistent with recent theory predicting more sexually concordant selection under environmental stress. Our results suggest an important role for precopulatory sexual selection in promoting thermal adaptation and evolutionary rescue.

Wolbachia-driven selective sweep in a range expanding insect species.

BACKGROUND: Evolutionary processes can cause strong spatial genetic signatures, such as local loss of genetic diversity, or conflicting histories from mitochondrial versus nuclear markers. Investigating these genetic patterns is important, as they may reveal obscured processes and players. The maternally inherited bacterium Wolbachia is among the most widespread symbionts in insects. Wolbachia typically spreads within host species by conferring direct fitness benefits, and/or by manipulating its host reproduction to favour infected over uninfected females. Under sufficient selective advantage, the mitochondrial haplotype associated with the favoured maternally-inherited symbiotic strains will spread (i.e. hitchhike), resulting in low mitochondrial genetic variation across the host species range. METHOD: The common bluetail damselfly (Ischnura elegans: van der Linden, 1820) has recently emerged as a model organism for genetics and genomic signatures of range expansion during climate change. Although there is accumulating data on the consequences of such expansion on the genetics of I. elegans, no study has screened for Wolbachia in the damselfly genus Ischnura. Here, we present the biogeographic variation in Wolbachia prevalence and penetrance across Europe and Japan (including samples from 17 populations), and from close relatives in the Mediterranean area (i.e. I. genei: Rambur, 1842; and I. saharensis: Aguesse, 1958). RESULTS: Our data reveal (a) multiple Wolbachia-strains, (b) potential transfer of the symbiont through hybridization, (c) higher infection rates at higher latitudes, and (d) reduced mitochondrial diversity in the north-west populations, indicative of hitchhiking associated with the selective sweep of the most common strain. We found low mitochondrial haplotype diversity in the Wolbachia-infected north-western European populations (Sweden, Scotland, the Netherlands, Belgium, France and Italy) of I. elegans, and, conversely, higher mitochondrial diversity in populations with low penetrance of Wolbachia (Ukraine, Greece, Montenegro and Cyprus). The timing of the selective sweep associated with infected lineages was estimated between 20,000 and 44,000 years before present, which is consistent with the end of the last glacial period about 20,000 years. CONCLUSIONS: Our findings provide an example of how endosymbiont infections can shape spatial variation in their host evolutionary genetics during postglacial expansion. These results also challenge population genetic studies that do not consider the prevalence of symbionts in many insects, which we show can impact geographic patterns of mitochondrial genetic diversity.

Correlational selection in the age of genomics.

Ecologists and evolutionary biologists are well aware that natural and sexual selection do not operate on traits in isolation, but instead act on combinations of traits. This long-recognized and pervasive phenomenon is known as multivariate selection, or-in the particular case where it favours correlations between interacting traits-correlational selection. Despite broad acknowledgement of correlational selection, the relevant theory has often been overlooked in genomic research. Here, we discuss theory and empirical findings from ecological, quantitative genetic and genomic research, linking key insights from different fields. Correlational selection can operate on both discrete trait combinations and quantitative characters, with profound implications for genomic architecture, linkage, pleiotropy, evolvability, modularity, phenotypic integration and phenotypic plasticity. We synthesize current knowledge and discuss promising research approaches that will enable us to understand how correlational selection shapes genomic architecture, thereby linking quantitative genetic approaches with emerging genomic methods. We suggest that research on correlational selection has great potential to integrate multiple fields in evolutionary biology, including developmental and functional biology, ecology, quantitative genetics, phenotypic polymorphisms, hybrid zones and speciation processes.

Genome assembly, sex-biased gene expression and dosage compensation in the damselfly Ischnura elegans.

The evolution of sex chromosomes, and patterns of sex-biased gene expression and dosage compensation, are poorly known among early winged insects such as odonates. We assembled and annotated the genome of Ischnura elegans (blue-tailed damselfly), which, like other odonates, has a male-hemigametic sex-determining system (X0 males, XX females). By identifying X-linked genes in I. elegans and their orthologs in other insect genomes, we found homologies between the X chromosome in odonates and chromosomes of other orders, including the X chromosome in Coleoptera. Next, we showed balanced expression of X-linked genes between sexes in adult I. elegans, i.e. evidence of dosage compensation. Finally, among the genes in the sex-determining pathway only fruitless was found to be X-linked, while only doublesex showed sex-biased expression. This study reveals partly conserved sex chromosome synteny and independent evolution of dosage compensation among insect orders separated by several hundred million years of evolutionary history.

A molecularphylogeny offorktail damselflies(genus Ischnura)revealsa dynamic macroevolutionary history of female colour polymorphisms.

Colour polymorphisms are popular study systems among biologists interested in evolutionary dynamics, genomics, sexual selection and sexual conflict. In many damselfly groups, such as in the globally distributed genus Ischnura (forktails), sex-limited female colour polymorphisms occur in multiple species. Female-polymorphic species contain two or three female morphs, one of which phenotypically matches the male (androchrome or male mimic) and the other(s) which are phenotypically distinct from the male (heterochrome). These female colour polymorphisms are thought to be maintained by frequency-dependent sexual conflict, but their macroevolutionary histories are unknown, due to the lack of a robust molecular phylogeny. Here, we present the first time-calibrated phylogeny of Ischnura, using a multispecies coalescent approach (StarBEAST2) and incorporating both molecular and fossil data for 41 extant species (55% of the genus). We estimate the age of Ischnura to be between 13.8 and 23.4 millions of years, i.e. Miocene. We infer the ancestral state of this genus as female monomorphism with heterochrome females, with multiple gains and losses of female polymorphisms, evidence of trans-species female polymorphisms and a significant positive relationship between female polymorphism incidence and current geographic range size. Our study provides a robust phylogenetic framework for future research on the dynamic macroevolutionary history of this clade with its extraordinary diversity of sex-limited female polymorphisms.

Extreme temperatures compromise male and female fertility in a large desert bird.

Temperature has a crucial influence on the places where species can survive and reproduce. Past research has primarily focused on survival, making it unclear if temperature fluctuations constrain reproductive success, and if so whether populations harbour the potential to respond to climatic shifts. Here, using two decades of data from a large experimental breeding programme of the iconic ostrich (Struthio camelus) in South Africa, we show that the number of eggs females laid and the number of sperm males produced were highly sensitive to natural temperature extremes (ranging from -5 °C to 45 °C). This resulted in reductions in reproductive success of up to 44% with 5 °C deviations from their thermal optimum. In contrast, gamete quality was largely unaffected by temperature. Extreme temperatures also did not expose trade-offs between gametic traits. Instead, some females appeared to invest more in reproducing at high temperatures, which may facilitate responses to climate change. These results show that the robustness of fertility to temperature fluctuations, and not just temperature increases, is a critical aspect of species persistence in regions predicted to undergo the greatest change in climate volatility.

Selection on phenotypic plasticity favors thermal canalization.

Climate change affects organisms worldwide with profound ecological and evolutionary consequences, often increasing population extinction risk. Climatic factors can increase the strength, variability, or direction of natural selection on phenotypic traits, potentially driving adaptive evolution. Phenotypic plasticity in relation to temperature can allow organisms to maintain fitness in response to increasing temperatures, thereby "buying time" for subsequent genetic adaptation and promoting evolutionary rescue. Although many studies have shown that organisms respond plastically to increasing temperatures, it is unclear if such thermal plasticity is adaptive. Moreover, we know little about how natural and sexual selection operate on thermal reaction norms, reflecting such plasticity. Here, we investigate how natural and sexual selection shape phenotypic plasticity in two congeneric and phenotypically similar sympatric insect species. We show that the thermal optima for longevity and mating success differ, suggesting temperature-dependent trade-offs between survival and reproduction in both sexes. Males in these species have similar thermal reaction norm slopes but have diverged in baseline body temperature (intercepts), being higher for the more northern species. Natural selection favored reduced thermal reaction norm slopes at high ambient temperatures, suggesting that the current level of thermal plasticity is maladaptive in the context of anthropogenic climate change and that selection now promotes thermal canalization and robustness. Our results show that ectothermic animals also at high latitudes can suffer from overheating and challenge the common view of phenotypic plasticity as being beneficial in harsh and novel environments.

The search for sexually antagonistic genes: Practical insights from studies of local adaptation and statistical genomics.

Sexually antagonistic (SA) genetic variation-in which alleles favored in one sex are disfavored in the other-is predicted to be common and has been documented in several animal and plant populations, yet we currently know little about its pervasiveness among species or its population genetic basis. Recent applications of genomics in studies of SA genetic variation have highlighted considerable methodological challenges to the identification and characterization of SA genes, raising questions about the feasibility of genomic approaches for inferring SA selection. The related fields of local adaptation and statistical genomics have previously dealt with similar challenges, and lessons from these disciplines can therefore help overcome current difficulties in applying genomics to study SA genetic variation. Here, we integrate theoretical and analytical concepts from local adaptation and statistical genomics research-including F ST and F IS statistics, genome-wide association studies, pedigree analyses, reciprocal transplant studies, and evolve-and-resequence experiments-to evaluate methods for identifying SA genes and genome-wide signals of SA genetic variation. We begin by developing theoretical models for between-sex F ST and F IS, including explicit null distributions for each statistic, and using them to critically evaluate putative multilocus signals of sex-specific selection in previously published datasets. We then highlight new statistics that address some of the limitations of F ST and F IS, along with applications of more direct approaches for characterizing SA genetic variation, which incorporate explicit fitness measurements. We finish by presenting practical guidelines for the validation and evolutionary analysis of candidate SA genes and discussing promising empirical systems for future work.

Male-Male Competition Causes Parasite-Mediated Sexual Selection for Local Adaptation.

AbstractSexual selection has been suggested to accelerate local adaptation and promote evolutionary rescue through several ecological and genetic mechanisms. Condition-dependent sexual selection has mainly been studied in laboratory settings, while data from natural populations are lacking. One ecological factor that can cause condition-dependent sexual selection is parasitism. Here, we quantified ectoparasite load (Arrenurus water mites) in a natural population of the common bluetail damselfly (Ischnura elegans) over 15 years. We quantified the strength of sexual selection against parasite load in both sexes and experimentally investigated the mechanisms behind such selection. Then we investigated how parasite resistance and tolerance changed over time to understand how they might influence population density. Parasites reduced mating success in both sexes, and sexual selection was stronger in males than in females. Experiments show that male-male competition is a strong force causing precopulatory sexual selection against parasite load. Although parasite resistance and male parasite tolerance increased over time, suggestive of increasing local adaptation against parasites, no signal of evolutionary rescue could be found. We suggest that condition-dependent sexual selection facilitates local adaptation against parasites and discuss its effects in evolutionary rescue.

Changes in gene expression during female reproductive development in a color polymorphic insect.

Pleiotropy (multiple phenotypic effects of single genes) and epistasis (gene interaction) have key roles in the development of complex phenotypes, especially in polymorphic taxa. The development of discrete and heritable phenotypic polymorphisms often emerges from major-effect genes that interact with other loci and have pleiotropic effects on multiple traits. We quantified gene expression changes during ontogenetic color development in a polymorphic insect (damselfly: Ischnura elegans), with three heritable female morphs, one being a male mimic. This female color polymorphism is maintained by male mating harassment and sexual conflict. Using transcriptome sequencing and de novo assembly, we demonstrate that all three morphs downregulate gene expression during early color development. The morphs become increasingly differentiated during sexual maturation and when developing adult coloration. These different ontogenetic trajectories arise because the male-mimic shows accelerated (heterochronic) development, compared to the other female morphs. Many loci with regulatory functions in reproductive development are differentially regulated in the male-mimic, including upstream and downstream regulators of ecdysone signaling and transcription factors potentially influencing sexual differentiation. Our results suggest that long-term sexual conflict does not only maintain this polymorphism, but has also modulated the evolution of gene expression profiles during color development of these sympatric female morphs.

Temperature drives pre-reproductive selection and shapes the biogeography of a female polymorphism.

Conflicts of interests between males and females over reproduction is a universal feature of sexually reproducing organisms and has driven the evolution of intersexual mimicry, mating behaviours and reproductive polymorphisms. Here, we show how temperature drives pre-reproductive selection in a female colour polymorphic insect that is subject to strong sexual conflict. These species have three female colour morphs, one of which is a male mimic. This polymorphism is maintained by frequency-dependent sexual conflict caused by male mating harassment. The frequency of female morphs varies geographically, with higher frequency of the male mimic at higher latitudes. We show that differential temperature sensitivity of the female morphs and faster sexual maturation of the male mimic increases the frequency of this morph in the north. These results suggest that sexual conflict during the adult stage is shaped by abiotic factors and frequency-independent pre-reproductive selection that operate earlier during ontogeny of these female morphs.

The odonate phenotypic database, a new open data resource for comparative studies of an old insect order.

We present The Odonate Phenotypic Database (OPD): an online data resource of dragonfly and damselfly phenotypes (Insecta: Odonata). Odonata is a relatively small insect order that currently consists of about 6400 species belonging to 32 families. The database consists of multiple morphological, life-history and behavioral traits, and biogeographical information collected from literature sources. We see taxon-specific phenotypic databases from Odonata and other organismal groups as becoming an increasing valuable resource in comparative studies. Our database has phenotypic records for 1011 of all 6400 known odonate species. The database is accessible at http://www.odonatephenotypicdatabase.org/, and a static version with an information file about the variables in the database is archived at Dryad.

Macroevolutionary Origin and Adaptive Function of a Polymorphic Female Signal Involved in Sexual Conflict.

Intersexual signals that reveal developmental or mating status in females have evolved repeatedly in many animal lineages. Such signals have functions in sexual conflict over mating and can therefore influence sexually antagonistic coevolution. However, we know little about how female signal development modifies male mating harassment and thereby sexual conflict. Here, we combine phylogenetic comparative analyses of a color polymorphic damselfly genus (Ischnura) with behavioral experiments in one target species to investigate the evolutionary origin and current adaptive function of a developmental female color signal. Many Ischnura species have multiple female color morphs, which include a male-colored morph (male mimics) and one or two female morphs that differ markedly from males (heterochrome females). In Ischnura elegans, males and male-mimicking females express a blue abdominal patch throughout postemergence life. Using phenotypic manipulations, we show that the developmental expression of this signaling trait in heterochrome females reduces premating harassment prior to sexual maturity. Across species this signal evolved repeatedly, but in heterochrome females its origin is contingent on the signal expressed by co-occurring male-mimicking females. Our results suggest that the co-option of a male-like trait to a novel female antiharassment function plays a key role in sexual conflict driven by premating interactions.