Supergenes promote ecological stasis in a keystone species.

Structural variation can create supergene architectures through tight genomic linkages that maintain traits in favourable combinations. A new study by Sodeland et al. links such supergenes in Atlantic cod with species persistence over millennia, despite the fisheries-induced decline in populations. This links intraspecific supergene diversity to ecological stasis, with significant consequences for ecosystem stability.

Environmental change unlinks a gene from its trait.

In Atlantic salmon (Salmo salar), sea age is a major life history trait governed by a sex-specific trade-off between reproductive success and survival. In this issue of Molecular Ecology, Besnier et al. (Molecular Ecology, 2023) found evidence to suggest that the disassociation between sea age and major effect loci, including the previously identified candidate genes vgll3 and six6, may be related to the recently observed trend towards slower growth and later maturation. These results are of importance because they challenge the prevailing view that evolution moves in a slow shuffle, and they provide a pertinent example of how an optimal phenotype can change due to growth-driven plasticity and lead to contemporary molecular and phenotypic evolution.

Morphology and metabolic traits related to swimming performance in Australasian snapper (Chrysophrys auratus) selected for fast growth.

Changes in body shape are linked to swimming performance and become relevant for selective breeding programmes in cultured finfish. We studied how the selection for fast growth could affect phenotypes by investigating the relationship between swimming performance and body shape. We also investigated how swimming might affect plasma metabolite concentrations. Critical swimming speed (UCrit), body traits (e.g., BW, body weight; BL, body length; K, condition factor), and plasma lactate and glucose concentrations were evaluated in two cohorts of Australasian snapper (Chrysophrys auratus): one derived from wild broodstock (F1), and the other selected for fast growth (F4). UCrit tests (n = 8) were applied in groups of 10 snapper of similar BW (71.7 g) and BL (14.6 cm). The absolute or relative UCrit values of both cohorts were similar (0.702 m⋅s-1 and 4.795 BL⋅s-1, respectively), despite the F4 cohort displaying a higher K. A positive correlation between K and absolute UCrit (Pearson's r = 0.414) was detected in the F4 cohort, but not in the F1 cohort, which may be linked to differences in body shape. A negative correlation between relative UCrit and body size (Pearson's r between -0.682 and -0.501), but no correlation between absolute UCrit and body size, was displayed in both cohorts. Plasma lactate and glucose concentrations were higher in the F4 cohort at UCrit. Whether a longer selective breeding programme could result in more changes in body shape, potentially affecting swimming performance, should be explored, along with the potential outcomes of the differences in metabolic traits detected.

A metabarcoding analysis of the wrackbed microbiome indicates a phylogeographic break along the North Sea-Baltic Sea transition zone.

Sandy beaches are biogeochemical hotspots that bridge marine and terrestrial ecosystems via the transfer of organic matter, such as seaweed (termed wrack). A keystone of this unique ecosystem is the microbial community, which helps to degrade wrack and re-mineralize nutrients. However, little is known about this community. Here, we characterize the wrackbed microbiome as well as the microbiome of a primary consumer, the seaweed fly Coelopa frigida, and examine how they change along one of the most studied ecological gradients in the world, the transition from the marine North Sea to the brackish Baltic Sea. We found that polysaccharide degraders dominated both microbiomes, but there were still consistent differences between wrackbed and fly samples. Furthermore, we observed a shift in both microbial communities and functionality between the North and Baltic Sea driven by changes in the frequency of different groups of known polysaccharide degraders. We hypothesize that microbes were selected for their abilities to degrade different polysaccharides corresponding to a shift in polysaccharide content in the different seaweed communities. Our results reveal the complexities of both the wrackbed microbial community, with different groups specialized to different roles, and the cascading trophic consequences of shifts in the near shore algal community.

Mitochondrial genomes reveal mid-Pleistocene population divergence, and post-glacial expansion, in Australasian snapper (Chrysophrys auratus).

Glacial cycles play important roles in determining the phylogeographic structure of terrestrial species, however, relatively little is known about their impacts on the distribution of marine biota. This study utilised modern (n = 350) and ancient (n = 26) mitochondrial genomes from Australasian snapper (Chrysophrys auratus) sampled in New Zealand to assess their demographic and phylogeographic history. We also tested for changes in genetic diversity using the up to 750-year-old mitochondrial genomes from pre-European archaeological sites to assess the potential impacts of human exploitation. Nucleotide diversity and haplotype diversity was high (π = 0.005, h = 0.972). There was no significant change in nucleotide diversity over the last 750 years (p = 0.343), with no detectable loss of diversity as a result of indigenous and industrial-scale fishing activity. While there was no evidence for contemporary population structure (AMOVA, p = 0.764), phylogeographic analyses identified two distinct mitochondrial clades that diverged approximately 650,000 years ago during the mid-Pleistocene, suggesting the species experienced barriers to gene flow when sea levels dropped over 120 m during previous glacial maxima. An exponential population increase was also observed around 8000 years ago consistent with a post-glacial expansion, which was likely facilitated by increased ocean temperatures and rising sea levels. This study demonstrates that glacial cycles likely played an important role in the demographic history of C. auratus and adds to our growing understanding of how dynamic climatic changes have influenced the evolution of coastal marine species.

Locally Adaptive Inversions Modulate Genetic Variation at Different Geographic Scales in a Seaweed Fly.

Across a species range, multiple sources of environmental heterogeneity, at both small and large scales, create complex landscapes of selection, which may challenge adaptation, particularly when gene flow is high. One key to multidimensional adaptation may reside in the heterogeneity of recombination along the genome. Structural variants, like chromosomal inversions, reduce recombination, increasing linkage disequilibrium among loci at a potentially massive scale. In this study, we examined how chromosomal inversions shape genetic variation across a species range and ask how their contribution to adaptation in the face of gene flow varies across geographic scales. We sampled the seaweed fly Coelopa frigida along a bioclimatic gradient stretching across 10° of latitude, a salinity gradient, and a range of heterogeneous, patchy habitats. We generated a chromosome-level genome assembly to analyze 1,446 low-coverage whole genomes collected along those gradients. We found several large nonrecombining genomic regions, including putative inversions. In contrast to the collinear regions, inversions and low-recombining regions differentiated populations more strongly, either along an ecogeographic cline or at a fine-grained scale. These genomic regions were associated with environmental factors and adaptive phenotypes, albeit with contrasting patterns. Altogether, our results highlight the importance of recombination in shaping adaptation to environmental heterogeneity at local and large scales.

Restricted X chromosome introgression and support for Haldane's rule in hybridizing damselflies.

Contemporary hybrid zones act as natural laboratories for the investigation of species boundaries and may shed light on the little understood roles of sex chromosomes in species divergence. Sex chromosomes are considered to function as a hotspot of genetic divergence between species; indicated by less genomic introgression compared to autosomes during hybridization. Moreover, they are thought to contribute to Haldane's rule, which states that hybrids of the heterogametic sex are more likely to be inviable or sterile. To test these hypotheses, we used contemporary hybrid zones of Ischnura elegans, a damselfly species that has been expanding its range into the northern and western regions of Spain, leading to chronic hybridization with its sister species Ischnura graellsii. We analysed genome-wide SNPs in the Spanish I. elegans and I. graellsii hybrid zone and found (i) that the X chromosome shows less genomic introgression compared to autosomes, and (ii) that males are underrepresented among admixed individuals, as predicted by Haldane's rule. This is the first study in Odonata that suggests a role of the X chromosome in reproductive isolation. Moreover, our data add to the few studies on species with X0 sex determination system and contradict the hypothesis that the absence of a Y chromosome causes exceptions to Haldane's rule.

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.

The genome of New Zealand trevally (Carangidae: Pseudocaranx georgianus) uncovers a XY sex determination locus.

BACKGROUND: The genetic control of sex determination in teleost species is poorly understood. This is partly because of the diversity of mechanisms that determine sex in this large group of vertebrates, including constitutive genes linked to sex chromosomes, polygenic constitutive mechanisms, environmental factors, hermaphroditism, and unisexuality. Here we use a de novo genome assembly of New Zealand silver trevally (Pseudocaranx georgianus) together with sex-specific whole genome sequencing data to detect sexually divergent genomic regions, identify candidate genes and develop molecular makers. RESULTS: The de novo assembly of an unsexed trevally (Trevally_v1) resulted in a final assembly of 579.4 Mb in length, with a N50 of 25.2 Mb. Of the assembled scaffolds, 24 were of chromosome scale, ranging from 11 to 31 Mb in length. A total of 28,416 genes were annotated after 12.8 % of the assembly was masked with repetitive elements. Whole genome re-sequencing of 13 wild sexed trevally (seven males and six females) identified two sexually divergent regions located on two scaffolds, including a 6 kb region at the proximal end of chromosome 21. Blast analyses revealed similarity between one region and the aromatase genes cyp19 (a1a/b) (E-value < 1.00E-25, identity > 78.8 %). Males contained higher numbers of heterozygous variants in both regions, while females showed regions of very low read-depth, indicative of male-specificity of this genomic region. Molecular markers were developed and subsequently tested on 96 histologically-sexed fish (42 males and 54 females). Three markers amplified in absolute correspondence with sex (positive in males, negative in females). CONCLUSIONS: The higher number of heterozygous variants in males combined with the absence of these regions in females support a XY sex-determination model, indicating that the trevally_v1 genome assembly was developed from a male specimen. This sex system contrasts with the ZW sex-determination model documented in closely related carangid species. Our results indicate a sex-determining function of a cyp19a1a-like gene, suggesting the molecular pathway of sex determination is somewhat conserved in this family. The genomic resources developed here will facilitate future comparative work, and enable improved insights into the varied sex determination pathways in teleosts. The sex marker developed in this study will be a valuable resource for aquaculture selective breeding programmes, and for determining sex ratios in wild populations.

Description of the growth hormone gene of the Australasian snapper, Chrysophrys auratus, and associated intra- and interspecific genetic variation.

The growth hormone (GH) gene of the marine teleost, the Australasian snapper (Chrysophrys auratus), was identified and characterized from the reference genome showing it was approximately 5577 bp in length and consisted of six exons and five introns. Large polymorphic repeat regions were found in the first and third introns, and putative transcription factor binding sites were identified. Phylogenetic analysis of the GH genes of perciform fish showed largely conserved coding regions and highly variable noncoding regions among species. Despite some exon sequence variation and an amino acid deletion identified between C. auratus and its sister species Chrysophrys/Pagrus major, the amino acid sequences and putative secondary structures were largely conserved across the Sparidae. A population-level assessment of 99 samples caught at five separate coastal locations in New Zealand revealed six variable alleles at the intron 1 site of the C. auratus GH gene. A population genetic analysis suggested that C. auratus from the five sample locations were largely panmictic, with no evidence for departure from the Hardy-Weinberg equilibrium, and have a high level of heterozygosity. Overall these results suggest that the GH gene is largely conserved across the coding regions, but some variability could be detected.

Detecting Polygenic Evolution: Problems, Pitfalls, and Promises.

Unraveling the genetic basis of organismal form and function remains one of the major goals of evolutionary biology. Theory has long supported a model of polygenic evolution in which quantitative traits are underpinned by many genes of small effect, but empirical methods have lacked the power to detect causative loci when effect sizes are small or moderate. We (i) review traditional approaches used for identifying the molecular basis of phenotypic traits, to highlight the inherent problems and pitfalls that bias them towards the detection of large-effect loci. We then (ii) outline the promises of recent statistical frameworks to detect polygenic signatures of trait evolution, and discuss some of the first studies in evolutionary biology employing these approaches. Lastly, we (iii) outline future directions and point to areas that still need development.

The genomic pool of standing structural variation outnumbers single nucleotide polymorphism by threefold in the marine teleost Chrysophrys auratus.

Recent studies have highlighted an important role of structural variation (SV) in ecological and evolutionary processes, but few have studied nonmodel species in the wild. As part of our long-term research programme on the nonmodel teleost fish Australasian snapper (Chrysophrys auratus), we aim to build one of the first catalogues of genomic variants (SNPs and indels, and deletions, duplications and inversions) in fishes and evaluate overlap of genomic variants with regions under putative selection (Tajima's D and π), and coding sequences (genes). For this, we analysed six males and six females from three locations in New Zealand and generated a high-resolution genomic variation catalogue. We characterized 20,385 SVs and found they intersected with almost a third of all annotated genes. Together with small indels, SVs account for three times more variation in the genome in terms of bases affected compared to SNPs. We found that a sizeable portion of detected SVs was in the upper and lower genomic regions of Tajima's D and π, indicating that some of these have an effect on the phenotype. Together, these results shed light on the often neglected genomic variation that is produced by SVs and highlights the need to go beyond the mere measure of SNPs when investigating evolutionary processes, such as species diversification and adaptation.

Intercontinental karyotype-environment parallelism supports a role for a chromosomal inversion in local adaptation in a seaweed fly.

Large chromosomal rearrangements are thought to facilitate adaptation to heterogeneous environments by limiting genomic recombination. Indeed, inversions have been implicated in adaptation along environmental clines and in ecotype specialization. Here, we combine classical ecological studies and population genetics to investigate an inversion polymorphism previously documented in Europe among natural populations of the seaweed fly Coelopa frigida along a latitudinal cline in North America. We test if the inversion is present in North America and polymorphic, assess which environmental conditions modulate the inversion karyotype frequencies, and document the relationship between inversion karyotype and adult size. We sampled nearly 2000 flies from 20 populations along several environmental gradients to quantify associations of inversion frequencies to heterogeneous environmental variables. Genotyping and phenotyping showed a widespread and conserved inversion polymorphism between Europe and America. Variation in inversion frequency was significantly associated with environmental factors, with parallel patterns between continents, indicating that the inversion may play a role in local adaptation. The three karyotypes of the inversion are differently favoured across micro-habitats and represent life-history strategies likely to be maintained by the collective action of several mechanisms of balancing selection. Our study adds to the mounting evidence that inversions are facilitators of adaptation and enhance within-species diversity.

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.

Balancing selection maintains cryptic colour morphs.

Animals display incredibly diverse colour patterns, a testament to evolution's endless innovation in shaping life. In many species, the interplay between males and females in the pursuit of mates has driven the evolution of a myriad of colour forms, from the flashy peacock tail feathers to the tiniest colour markings in damselflies. In others, colour provides crypsis by allowing to blend into the background and to escape the eyes of predators. While the obvious benefits of this dazzling diversity for reproduction and survival seem straightforward, its maintenance is not. Theory predicts that genetic drift and various forms of selection reduce variation over time, making the persistence of colour variants over generations a puzzle. In this issue of Molecular Ecology, Lindtke et al. () study the cryptic colour morphs of Timema cristinae walking sticks to shed light on the genetic architecture and mechanisms that allow colour polymorphism maintenance over long timescales. By combining genome-wide data with phenotyping information from natural populations, they were able to map the green and melanistic colour to one genomic region with highly reduced effective recombination rate between two main chromosomal variants, consistent with an inversion polymorphism. These two main chromosomal variants showed geographically widespread heterozygote excess, and genomic signatures consistent with long-term balancing selection. A younger chromosomal variant was detected for the third morph, the green-striped colour morphs, in the same genomic regions as the melanistic and the green-unstriped morphs. Together, these results suggest that the genetic architecture of cryptic T. cristinae morphs is caused by nonrecombining genomic blocks that have been maintained over extended time periods by balancing selection making this study one of the few available empirical examples documenting that balancing selection of various forms may play an important role in maintaining adaptive genetic variation in nature.

Fifteen years of quantitative trait loci studies in fish: challenges and future directions.

Understanding the genetic basis of phenotypic variation is a major challenge in biology. Here, we systematically evaluate 146 quantitative trait loci (QTL) studies on teleost fish over the last 15 years to investigate (i) temporal trends and (ii) factors affecting QTL detection and fine-mapping. The number of fish QTL studies per year increased over the review period and identified a cumulative number of 3632 putative QTLs. Most studies used linkage-based mapping approaches and were conducted on nonmodel species with limited genomic resources. A gradual and moderate increase in the size of the mapping population and a sharp increase in marker density from 2011 onwards were observed; however, the number of QTLs and variance explained by QTLs changed only minimally over the review period. Based on these findings, we discuss the causative factors and outline how larger sample sizes, phenomics, comparative genomics, epigenetics and software development could improve both the quantity and quality of QTLs in future genotype-phenotype studies. Given that the technical limitations on DNA sequencing have mostly been overcome in recent years, a renewed focus on these and other study design factors will likely lead to significant improvements in QTL studies in the future.

Transcriptome profiling in the damselfly Ischnura elegans identifies genes with sex-biased expression.

BACKGROUND: Sexual dimorphism occurs widely across the animal kingdom and has profound effects on evolutionary trajectories. Here, we investigate sex-specific gene expression in Ischnura elegans (Odonata: dragonflies and damselflies), a species with pronounced sexual differences including a female-limited colour polymorphism with two female-like gynochrome morphs and one male-mimicking, androchrome morph. Whole-organism transcriptome profiling and sex-biased gene expression analysis was conducted on adults of both sexes (pooling all females as well as separating the three morphs) to gain insights into genes and pathways potentially associated with sexual development and sexual conflict. RESULTS: The de novo transcriptome assembly was of high quality and completeness (54 k transcripts; 99.6% CEGMA score; 55% annotated). We identified transcripts of several relevant pathways, including transcripts involved in sex determination, hormone biosynthesis, pigmentation and innate immune signalling. A total of 1,683 genes were differentially expressed (DE) between males and all females (1,173 were female-biased; 510 male-biased). The DE genes were associated with sex-specific physiological and reproductive processes, olfaction, pigmentation (ommochrome and melanin), hormone (ecdysone) biosynthesis and innate immunity signalling pathways. Comparisons between males and each female morph category showed that the gynochromes differed more from males than the androchrome morph. CONCLUSIONS: This is the first study to characterize sex-biased gene expression in odonates, one of the most ancient extant insect orders. Comparison between I. elegans sexes revealed expression differences in several genes related to sexual differences in behaviour and development as well as morphology. The differential expression of several olfactory genes suggests interesting sexual components in the detection of odours, pheromones and environmental volatiles. Up-regulation of pigmentation pathways in females indicates a prominent role of ommochrome pigments in the formation of the genetically controlled female colour polymorphism. Finally, the female-biased expression of several immunity genes suggests a stronger immune response in females, possibly related to the high levels of male mating harassment and recurrent matings in this species, both of which have been shown to injure females and expose them to sexually transmitted diseases and toxins contained in seminal fluids.

Gene expression under thermal stress varies across a geographical range expansion front.

Many ectothermic species are currently expanding their distributions polewards due to anthropogenic global warming. Molecular genetic mechanisms facilitating range expansion under these conditions are largely unknown, but understanding these could help mitigate expanding pests and disease vectors, or help explain why some species fail to track changing climates. Here, using RNA-seq data, we examine genomewide changes in gene expression under heat and cold stress in the range-expanding damselfly Ischnura elegans in northern Europe. We find that both the number of genes involved and levels of gene expression under heat stress have become attenuated during the expansion, consistent with a previously reported release from selection on heat tolerances as species move polewards. Genes upregulated under cold stress differed between core and edge populations, corroborating previously reported rapid adaptation to cooler climates at the expansion front. Expression of sixty-nine genes exhibited a region x treatment effect; these were primarily upregulated in response to heat stress in core populations but in response to cold stress at the range edge, suggesting that some cellular responses originally adapted to heat stress may switch to cold-stress functionality upon encountering novel thermal selection regimes during range expansion. Transcriptional responses to thermal stress involving heat-shock and neural function genes were largely geographically conserved, while retrotransposon, regulatory, muscle function and defence gene expression patterns were more variable. Flexible mechanisms of cold-stress response and the ability of some genes to shift their function between heat and cold stress might be key mechanisms facilitating rapid poleward expansion in insects.

Odonata (dragonflies and damselflies) as a bridge between ecology and evolutionary genomics.

Odonata (dragonflies and damselflies) present an unparalleled insect model to integrate evolutionary genomics with ecology for the study of insect evolution. Key features of Odonata include their ancient phylogenetic position, extensive phenotypic and ecological diversity, several unique evolutionary innovations, ease of study in the wild and usefulness as bioindicators for freshwater ecosystems worldwide. In this review, we synthesize studies on the evolution, ecology and physiology of odonates, highlighting those areas where the integration of ecology with genomics would yield significant insights into the evolutionary processes that would not be gained easily by working on other animal groups. We argue that the unique features of this group combined with their complex life cycle, flight behaviour, diversity in ecological niches and their sensitivity to anthropogenic change make odonates a promising and fruitful taxon for genomics focused research. Future areas of research that deserve increased attention are also briefly outlined.