Plasticity and associated epigenetic mechanisms play a role in thermal evolution during range expansion.

Due to global change, many species are shifting their distribution and are thereby confronted with novel thermal conditions at the moving range edges. Especially during the initial phases of exposure to a new environment, it has been hypothesized that plasticity and associated epigenetic mechanisms enable species to cope with environmental change. We tested this idea by capitalizing on the well-documented southward range expansion of the damselfly Ischnura elegans from France into Spain where the species invaded warmer regions in the 1950s in eastern Spain (old edge region) and in the 2010s in central Spain (new edge region). Using a common garden experiment at rearing temperatures matching the ancestral and invaded thermal regimes, we tested for evolutionary changes in (thermal plasticity in) larval life history and heat tolerance in these expansion zones. Through the use of de- and hypermethylating agents, we tested whether epigenetic mechanisms play a role in enabling heat tolerance during expansion. We used the phenotype of the native sister species in Spain, I. graellsii, as proxy for the locally adapted phenotype. New edge populations converged toward the phenotype of the native species through plastic thermal responses in life history and heat tolerance while old edge populations (partly) constitutively evolved a faster life history and higher heat tolerance than the core populations, thereby matching the native species. Only the heat tolerance of new edge populations increased significantly when exposed to the hypermethylating agent. This suggests that the DNA methylation machinery is more amenable to perturbation at the new edge and shows it is able to play a role in achieving a higher heat tolerance. Our results show that both (evolved) plasticity as well as associated epigenetic mechanisms are initially important when facing new thermal regimes but that their importance diminishes with time.

The evolutionary outcomes of climate-change-induced hybridization in insect populations.

Rapid range shifts are one of the most frequent responses to climate change in insect populations. Climate-induced range shifts can lead to the breakdown of isolation barriers, and thus, to an increase in hybridization and introgression. Long-term evolutionary consequences such as the formation of hybrid zones, introgression, speciation, and extinction have been predicted as a result of climate-induced hybridization. Our review shows that there has been an increase in the number of published cases of climate-induced hybridization in insects, and that the formation of hybrid zones and introgression seems to be, at the moment, the most frequent outcomes. Although introgression is considered positive, since it increases species' genetic diversity, in the long term, it could lead to negative outcomes such as species fusion or genetic swamping.

Convergence of life history and physiology during range expansion toward the phenotype of the native sister species.

In our globally changing planet many species show range expansions whereby they encounter new thermal regimes that deviate from those of their source region. Pressing questions are to what extent and through which mechanisms, plasticity and/or evolution, species respond to the new thermal regimes and whether these trait changes are adaptive. Using a common-garden experiment, we tested for plastic and evolutionary trait changes in life history and a set of understudied biochemical/physiological traits during the range expansion of the damselfly Ischnura elegans from France into a warmer region in Spain. To assess the adaptiveness of the trait changes we used the phenotype of its native sister species in Spain, I. graellsii, as proxy for the locally adapted phenotype. While our design cannot fully exclude maternal effects, our results suggest that edge populations adapted to the local conditions in the newly invaded region through the evolution of a faster pace-of-life (faster development and growth rates), a smaller body size, a higher energy budget and increased expression levels of the heat shock gene DnaJ. Notably, based on convergence toward the phenotype of the native sister species and its thermal responses, and the fit with predictions of life history theory these potential evolutionary changes were likely adaptive. Nevertheless, the convergence toward the native sister species is incomplete for thermal plasticity in traits associated with anaerobic metabolism and melanization. Our results highlight that evolution might at least partly contribute in an adaptive way to the persistence of populations during range expansion into new thermal environments and should be incorporated when predicting and understanding species' range expansions.

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.

Insect responses to heat: physiological mechanisms, evolution and ecological implications in a warming world.

Surviving changing climate conditions is particularly difficult for organisms such as insects that depend on environmental temperature to regulate their physiological functions. Insects are extremely threatened by global warming, since many do not have enough physiological tolerance even to survive continuous exposure to the current maximum temperatures experienced in their habitats. Here, we review literature on the physiological mechanisms that regulate responses to heat and provide heat tolerance in insects: (i) neuronal mechanisms to detect and respond to heat; (ii) metabolic responses to heat; (iii) thermoregulation; (iv) stress responses to tolerate heat; and (v) hormones that coordinate developmental and behavioural responses at warm temperatures. Our review shows that, apart from the stress response mediated by heat shock proteins, the physiological mechanisms of heat tolerance in insects remain poorly studied. Based on life-history theory, we discuss the costs of heat tolerance and the potential evolutionary mechanisms driving insect adaptations to high temperatures. Some insects may deal with ongoing global warming by the joint action of phenotypic plasticity and genetic adaptation. Plastic responses are limited and may not be by themselves enough to withstand ongoing warming trends. Although the evidence is still scarce and deserves further research in different insect taxa, genetic adaptation to high temperatures may result from rapid evolution. Finally, we emphasize the importance of incorporating physiological information for modelling species distributions and ecological interactions under global warming scenarios. This review identifies several open questions to improve our understanding of how insects respond physiologically to heat and the evolutionary and ecological consequences of those responses. Further lines of research are suggested at the species, order and class levels, with experimental and analytical approaches such as artificial selection, quantitative genetics and comparative analyses.

PRDM9 Diversity at Fine Geographical Scale Reveals Contrasting Evolutionary Patterns and Functional Constraints in Natural Populations of House Mice.

One of the major challenges in evolutionary biology is the identification of the genetic basis of postzygotic reproductive isolation. Given its pivotal role in this process, here we explore the drivers that may account for the evolutionary dynamics of the PRDM9 gene between continental and island systems of chromosomal variation in house mice. Using a data set of nearly 400 wild-caught mice of Robertsonian systems, we identify the extent of PRDM9 diversity in natural house mouse populations, determine the phylogeography of PRDM9 at a local and global scale based on a new measure of pairwise genetic divergence, and analyze selective constraints. We find 57 newly described PRDM9 variants, this diversity being especially high on Madeira Island, a result that is contrary to the expectations of reduced variation for island populations. Our analysis suggest that the PRDM9 allelic variability observed in Madeira mice might be influenced by the presence of distinct chromosomal fusions resulting from a complex pattern of introgression or multiple colonization events onto the island. Importantly, we detect a significant reduction in the proportion of PRDM9 heterozygotes in Robertsonian mice, which showed a high degree of similarity in the amino acids responsible for protein-DNA binding. Our results suggest that despite the rapid evolution of PRDM9 and the variability detected in natural populations, functional constraints could facilitate the accumulation of allelic combinations that maintain recombination hotspot symmetry. We anticipate that our study will provide the basis for examining the role of different PRDM9 genetic backgrounds in reproductive isolation in natural populations.

Molecular and ecological signatures of an expanding hybrid zone.

Many species are currently changing their distributions and subsequently form sympatric zones with hybridization between formerly allopatric species as one possible consequence. The damselfly Ischnura elegans has recently expanded south into the range of its ecologically and morphologically similar sister species Ischnura graellsii. Molecular work shows ongoing introgression between these species, but the extent to which this species mixing is modulated by ecological niche use is not known. Here, we (1) conduct a detailed population genetic analysis based on molecular markers and (2) model the ecological niche use of both species in allopatric and sympatric regions. Population genetic analyses showed chronic introgression between I. elegans and I. graellsii across a wide part of Spain, and admixture analysis corroborated this, showing that the majority of I. elegans from the sympatric zone could not be assigned to either the I. elegans or I. graellsii species cluster. Niche modeling demonstrated that I. elegans has modified its environmental niche following hybridization and genetic introgression with I. graellsii, making niche space of introgressed I. elegans populations more similar to I. graellsii. Taken together, this corroborates the view that adaptive introgression has moved genes from I. graellsii into I. elegans and that this process is enabling Spanish I. elegans to occupy a novel niche, further facilitating its expansion. Our results add to the growing evidence that hybridization can play an important and creative role in the adaptive evolution of animals.

The evolutionary history of colour polymorphism in Ischnura damselflies.

A major challenge in evolutionary biology consists of understanding how genetic and phenotypic variation is created and maintained. In this study, we investigated the origin(s) and evolutionary patterns of the female-limited colour polymorphism in ischnuran damselflies. These consist of the presence of one to three colour morphs: one androchrome morph with a coloration that is similar to the male and two gynochrome morphs (infuscans and aurantiaca) with female-specific coloration. We (i) documented the colour and mating system of 44 of the 75 taxa within the genus Ischnura, (ii) reconstructed the evolutionary history of colour and mating system to identify the ancestral state, (iii) evaluated the stability of the colour morph status over time and (iv) tested for a correlation between colour and mating system. We found that the ancestral female colour of Ischnura was monomorphic and aurantiaca and that colour morph status changed over time, characterized by many gains and losses across the species tree. Our results further showed that colour polymorphism is significantly more frequent among polyandric species, whereas monandric species tend to be monomorphic. Research on some Ischnura species has shown that colour morphs have evolved to reduce male mating harassment, and our finding that the same phenotypic morphs have evolved multiple times (convergent evolution) suggests that several species in this genus might be experiencing similar selective pressures.

Alternative reproductive strategies and the maintenance of female color polymorphism in damselflies.

Genetic polymorphisms are powerful model systems to study the maintenance of diversity in nature. In some systems, polymorphisms are limited to female coloration; these are thought to have arisen as a consequence of reducing male mating harassment, commonly resulting in negative frequency-dependent selection on female color morphs. One example is the damselfly Ischnura elegans, which shows three female color morphs and strong sexual conflict over mating rates. Here, we present research integrating male tactics, and female evolutionary strategies (female mating behavior and morph-specific female fecundity) in populations with different morph-specific mating frequencies, to obtain an understanding of mating rates in nature that goes beyond the mere measure of color frequencies. We found that female morph behavior differed significantly among but not within morphs (i.e., female morph behavior was fixed). In contrast, male tactics were strongly affected by the female morph frequency in the population. Laboratory work comparing morph-specific female fecundity revealed that androchrome females have lower fecundity than both of the gynochrome female morphs in the short term (3-days), but over a 10-day period one of the gynochrome female morphs became more fecund than either of the other morphs. In summary, our study found sex-specific dynamics in response to different morph frequencies and also highlights the importance of studying morph-specific fecundities across different time frames to gain a better understanding of the role of alternative reproductive strategies in the maintenance of female-limited color polymorphism.

Evolutionary consequences of climate-induced range shifts in insects.

Range shifts can rapidly create new areas of geographic overlap between formerly allopatric taxa and evidence is accumulating that this can affect species persistence. We review the emerging literature on the short- and long-term consequences of these geographic range shifts. Specifically, we focus on the evolutionary consequences of novel species interactions in newly created sympatric areas by describing the potential (i) short-term processes acting on reproductive barriers between species and (ii) long-term consequences of range shifts on the stability of hybrid zones, introgression and ultimately speciation and extinction rates. Subsequently, we (iii) review the empirical literature on insects to evaluate which processes have been studied, and (iv) outline some areas that deserve increased attention in the future, namely the genomics of hybridisation and introgression, our ability to forecast range shifts and the impending threat from insect vectors and pests on biodiversity, human health and crop production. Our review shows that species interactions in de novo sympatric areas can be manifold, sometimes increasing and sometimes decreasing species diversity. A key issue that emerges is that climate-induced hybridisations in insects are much more widespread than anticipated and that rising temperatures and increased anthropogenic disturbances are accelerating the process of species mixing. The existing evidence only shows the tip of the iceberg and we are likely to see many more cases of species mixing following range shifts in the near future.

Introgression and rapid species turnover in sympatric damselflies.

BACKGROUND: Studying contemporary hybridization increases our understanding of introgression, adaptation and, ultimately, speciation. The sister species Ischnura elegans and I. graellsii (Odonata: Coenagrionidae) are ecologically, morphologically and genetically similar and hybridize. Recently, I. elegans has colonized northern Spain, creating a broad sympatric region with I. graellsii. Here, we review the distribution of both species in Iberia and evaluate the degree of introgression of I. graellsii into I. elegans using six microsatellite markers (442 individuals from 26 populations) and five mitochondrial genes in sympatric and allopatric localities. Furthermore, we quantify the effect of hybridization on the frequencies of the genetically controlled colour polymorphism in females of both species. RESULTS: In a principal component analysis of the microsatellite data, the first two principal components summarised almost half (41%) of the total genetic variation. The first axis revealed a clear separation of I. graellsii and I. elegans populations, while the second axis separated I. elegans populations. Admixture analyses showed extensive hybridization and introgression in I. elegans populations, consistent with I. elegans backcrosses and occasional F1-hybrids, suggesting hybridization is on-going. More specifically, approximately 58% of the 166 Spanish I. elegans individuals were assigned to the I. elegans backcross category, whereas not a single of those individuals was assigned to the backcross with I. graellsii. The mitochondrial genes held little genetic variation, and the most common haplotype was shared by the two species. CONCLUSIONS: The results suggest rapid species turnover in sympatric regions in favour of I. elegans, corroborating previous findings that I. graellsii suffers a mating disadvantage in sympatry with I. elegans. Examination of morph frequency dynamics indicates that hybridization is likely to have important implications for the maintenance of multiple female morphs, in particular during the initial period of hybridization.

Environmental and climatic determinants of molecular diversity and genetic population structure in a coenagrionid damselfly.

Identifying environmental factors that structure intraspecific genetic diversity is of interest for both habitat preservation and biodiversity conservation. Recent advances in statistical and geographical genetics make it possible to investigate how environmental factors affect geographic organisation and population structure of molecular genetic diversity within species. Here we present a study on a common and wide ranging insect, the blue tailed damselfly Ischnuraelegans, which has been the target of many ecological and evolutionary studies. We addressed the following questions: (i) Is the population structure affected by longitudinal or latitudinal gradients?; (ii) Do geographic boundaries limit gene flow?; (iii) Does geographic distance affect connectivity and is there a signature of past bottlenecks?; (iv) Is there evidence of a recent range expansion and (vi) what is the effect of geography and climatic factors on population structure? We found low to moderate genetic sub-structuring between populations (mean F(ST) = 0.06, D(est) = 0.12), and an effect of longitude, but not latitude, on genetic diversity. No significant effects of geographic boundaries (e.g. water bodies) were found. F(ST)-and D(est)-values increased with geographic distance; however, there was no evidence for recent bottlenecks. Finally, we did not detect any molecular signatures of range expansions or an effect of geographic suitability, although local precipitation had a strong effect on genetic differentiation. The population structure of this small insect has probably been shaped by ecological factors that are correlated with longitudinal gradients, geographic distances, and local precipitation. The relatively weak global population structure and high degree of genetic variation within populations suggest that I. elegans has high dispersal ability, which is consistent with this species being an effective and early coloniser of new habitats.