Signatures of past changes in population size have been detected in genome-wide variation in many species. However, the causes of such demographic changes and the extent to which they are shared across co-distributed species remain poorly understood. During Pleistocene glacial maxima, many temperate European species were confined to southern refugia. While vicariance and range expansion processes associated with glacial cycles have been widely studied, little is known about the demographic history of refugial populations, and the extent and causes of demographic variation among co-distributed species. We used whole genome sequence data to reconstruct and compare demographic histories during the Quaternary for Iberian refuge populations in a single ecological guild (seven species of chalcid parasitoid wasps associated with oak cynipid galls). We find support for large changes in effective population size through the Pleistocene that coincide with major climate events. However, there is little evidence that the timing, direction and magnitude of demographic change are shared across species, suggesting that demographic histories are largely idiosyncratic even at the scale of a single glacial refugium.

Deciduous forests form the dominant natural vegetation of Europe today, but were restricted to small refugia during Pleistocene cold stages, implying an evolutionary past shaped by recurrent range contractions and expansions. Cold-stage forest refugia were probably widespread in southern and central Europe, with the northwestern Balkan Peninsula being of particular importance. However, the actual number and location of deciduous forest refugia, as well as the connections between them, remain disputed. Here, we address the evolutionary dynamics of the deciduous forest understorey species Euphorbia carniolica as a proxy for past forest dynamics. To do so, we obtained genomic and morphometric data from populations representing the species' entire range, investigated phylogenetic position and intraspecific genetic variation, tested explicit demographic scenarios and applied species distribution models. Our data support two disjoint groups linked to separate refugia on the northwestern and central Balkan Peninsula. We find that genetic differentiation between groups started in the early Pleistocene via vicariance, suggesting a larger distribution in the past. Both refugia acted as sources for founder events to the southeastern Alps and the Carpathians, whereas the latter were likely colonized before the last cold stage. In line with traditional views on the pre-Pleistocene origin of many southeastern European deciduous forest species, the origin of E. carniolica was dated to the late Pliocene. The fact that E. carniolica evolved at a time when a period of continuous forestation was ending in much of Eurasia provides an interesting biogeographical perspective on the past links between Eurasian deciduous forests and their biota.

Secondary contact of species that have evolved partial reproductive isolation in allopatry may result in several outcomes, which range from rampant hybridization to barrier reinforcement. Reinforcement arises from reduced hybrid fitness, which promotes assortative mating and hence speciation. In plants, self-fertilization and disjunction in reproductive phenology are often cited as evidence of reinforcement. However, local adaptation and pleiotropic effects during colonization can also lead to reproductive isolation without reinforcement. We explored these competing possibilities in a fir species complex (Abies flinckii - A. religiosa) distributed in ‘sky-islands’ along the Trans-Mexican Volcanic Belt (TMVB), in central Mexico. Despite co-occurring in two independent sympatric regions (west and center), these two taxa seem to rarely interbreed because of disjunct reproductive phenologies. We genotyped 1,147 SNPs, generated by GBS across 23 populations, and compared multiple demographic scenarios, built based on the geological history of the TMVB. The best-fitting model revealed one of the most rapid and complete speciation cases for a conifer species-pair, dating back to ~1.2 Ma, which included an early asymmetric gene flow (mostly from A. flinckii into A. religiosa) limited to the most ancient sympatric region. Coupled with the lack of support for colonization models, our demographic inferences point to an early development of reinforcement, as a putative mechanism for avoiding hybridization. Reinforcement should be considered as a key player for originating and maintaining species diversity in the tropics and subtropics and incorporated in studies with other model systems.

Low vagility species may hold strong genetic signatures of past biogeographic processes but are also vulnerable to habitat loss. Flightless grasshoppers of the morabine group were once widespread in south-eastern Australia including Tasmania but are becoming restricted to remnant patches of vegetation, with local ranges impacted by agriculture and development as well as management. Habitat fragmentation can generate genetically differentiated “island” populations with low genetic variation. However, following revegetation, populations could be re-established and gene flow increased. Here we characterise SNP based genetic variation in a widespread chromosomal race of the morabine Vandiemenella viatica (race 19) to investigate the genetic health of remnant populations and to provide guidelines for restoration efforts. We update the distribution of this race to new sites in Victoria and Tasmania, and show that V. viatica populations from northern Tasmania and eastern Victoria have reduced genetic variation compared to other mainland populations. In contrast there was no effect of habitat fragment size on genetic variation. Tasmanian V. viatica populations fell into two groups, one connected genetically to eastern Victoria and the other connected to south-western Victoria. Mainland populations showed isolation by distance. These patterns are consistent with expectations from past biogeographic processes rather than local recent population fragmentation and emphasize the importance of small local reserves in preserving genetic variation. The study highlights how genomic analyses can combine information on genetic variability and population structure to identify biogeographic patterns within a species, which in turn can inform decisions on potential source populations for translocations.

Geographically connected species pairs with weakly differentiated genomes could either represent cases of genomic homogenization in progress or of incipient parapatric speciation. Discriminating between these processes is difficult because intermediate stages of either may produce weakly differentiated genomes that diverge at few locations. We used coalescent modelling applied to a genome-wide sample of SNPs to discriminate between speciation with gene flow and genomic homogenization in two phenotypically distinct but genomically weakly diverged species of elevationally replacing Ramphocelus tanagers, forming a hybrid zone in the Andean foothills. We found overwhelming support for a model of genomic homogenization following secondary contact. Simulating under this model suggested that our species pair was differentiated (FST = 0.30) at secondary contact but that most of the genome has rapidly homogenized during 254 Ky of high gene flow towards the present (FST = 0.02). Despite extensive genome-wide homogenization, plumage remains distinctive with a narrower than expected geographic cline width, indicating divergent selection on colour. We found two SNPs significantly associated with plumage colour, which retain moderately high FST. We conclude that the majority of the genome has fused, but that divergent selection on select loci probably maintains the geographically structured colour differences between these incipient species.

As sea surface temperature increases, many coral species that used to harbor symbionts of the genus Cladocopium have become colonized with the thermally tolerant genus, Durusdinium. Here, we asked how symbionts of one genus react to the presence of another symbiont genus within the same coral host, and what effect this has on the host. We used previously published data from Acropora hyacinthus corals hosting Cladocopium and/or Durusdinium symbionts and looked at gene expression in all three symbiotic partners depending on the relative proportions of symbiont genera within the host. We find that both Cladocopium and Durusdinium change their expression most when their proportions are nearly equal (the state that we call “codominance”): both genera elevate expression of photosynthesis and ribosomal genes, suggesting increase in photosynthesis and growth (i.e. higher productivity). At the same time, the coral host also elevates production of ribosomes suggesting faster cellular growth, and, when heated, shows less pronounced stress response. These results can be explained in two ways. One explanation is that increased competition between symbionts heightens their productivity, which benefits the host, making it more resilient to stress. Alternatively, the symbionts’ elevated productivity might be the consequence of the host being particularly healthy. Under this explanation, rapid growth of the healthy host creates new space, lowering the symbionts’ competition and allowing for codominance. The latter explanation is supported by the fact that codominance is associated with lower symbiont densities. Irrespective of the causation, the presence of mixed symbiont communities could potentially be used as an instant indicator of coral well-being, which would be a useful tool for coral conservation and restoration.

Telomerase activity and telomere maintenance in certain somatic cells of human adults support the proliferative capacity of these cells and thus contribute to their regenerative potential, and telomerase activity and telomere length are commonly considered lifespan predictors. Eusocial insects provide excellent models for aging research based on their extraordinary caste-related lifespan differences that contradict the typical mammalian fecundity/lifespan trade-off. Telomerase activity is upregulated in the reproductive, long-lived individuals of eusocial insects such as queens and kings, and telomerase activity may act as a key factor in their extended longevity. But, as documented by the presence of telomerase in somatic tissues of numerous invertebrate and vertebrate species, the connection between telomerase activity and the predicted lifespan is not clear. Here, I ask whether somatic telomerase activity in eusocial reproductives may serve its non-canonical function to protect its individuals against the metabolic stress due to reproduction and reflect a more common phenomenon among species. Here, I propose a hypothesis that the presence of telomerase activity in somatic cells reflects a different reproduction strategy of species.

Phytoplankton have short generation times, flexible reproduction strategies, large population sizes, and high standing genetic diversity, traits that should facilitate rapid evolution under directional selection. We quantified local adaptation of copper tolerance in a population of the diatom Skeletonema marinoi from a mining exposed inlet in the Baltic Sea and in a non-exposed population 100 km away. We hypothesized that mining pollution has driven evolution of elevated copper tolerance in the impacted population of S. marinoi. Assays of 58 strains originating from sediment resting stages revealed no difference in the average tolerance to copper between the two populations. However, variation within populations was greater at the mining site, with three strains displaying hyper-tolerant phenotypes. In an artificial evolution experiment, we used a novel intraspecific metabarcoding locus to track selection and quantify fitness of all 58 strains during co-cultivation in one control and one toxic copper treatment. As expected, the hyper-tolerant strains enabled rapid evolution of copper tolerance in the mining exposed population through selection on available strain diversity. Within 42 days, in each experimental replicate a single strain dominated (30-99% abundance) but different strains dominated the different treatments. The reference population developed tolerance beyond expectations primarily due to slowly developing plastic response in one strain, suggesting that different modes of copper tolerance are present in the two populations. Our findings provide novel empirical evidence that standing genetic diversity of phytoplankton resting stage allows populations to evolve rapidly (20-50 generations) and flexibly on timescales relevant for seasonal bloom progressions.

Photosymbiodemes are a special case of lichen symbiosis where one lichenized fungus engages in symbiosis with two different photosynthetic partners, a cyanobacterium and a green alga, to develop two distinctly looking photomorphs. We investigated differential gene expression in photosymbiodemes of the lichen Peltigera britannica at different temperatures representing mild and putatively stressful conditions and compared gene expression of thallus sectors containing cyanobacterial photobionts with thallus sectors with both green algal and cyanobacterial photobionts. Firstly, because of known ecological differences between photomorphs, we investigated symbiont-specific responses in gene expression to temperature increases. Secondly, we quantified photobiont-mediated differences in fungal gene expression. High temperatures expectedly led to an upregulation of genes involved in heat shock responses in all organisms in whole transcriptome data. As expected, the expression of genes involved in photosynthesis was increased in both photobiont types at 15 and 25 °C. The green algae exhibited thermal stress responses mainly at 25 °C, the fungus and the cyanobacteria already at 15 °C, demonstrating symbiont-specific responses to environmental cues and symbiont-specific ecological optima. Furthermore, photobiont-mediated differences in fungal gene expression could be identified, with upregulation of distinct biological processes in the different morphs, showing that interaction with specific symbiosis partners profoundly impacts fungal gene expression.

Hybridization plays an important and underappreciated role in shaping the evolutionary trajectories of species. Following the introduction of a non-native organism to a novel habitat, hybridization with a native congener may affect the probability of establishment of the introduced species. In most documented cases of hybridization between a native and a non-native species, a mosaic hybrid zone is formed, with hybridization occurring heterogeneously across the landscape. In contrast, most naturally occurring hybrid zones are clinal in structure. Here we report on a long-term microsatellite dataset that monitored hybridization between the invasive winter moth, Operophtera brumata (Lepidoptera: Geometridae), and the native Bruce spanworm, O. bruceata, over a 12-year period. Our results document one of the first examples of the real-time formation and geographic settling of a clinal hybrid zone. In addition, by comparing one transect in Massachusetts where extreme winter cold temperatures have been hypothesized to restrict the distribution of winter moth, and one in coastal Connecticut, where winter temperatures are moderated by Long Island Sound, we find that the location of the hybrid zone appears to be independent of environmental variables and maintained under a tension model wherein the stability of the hybrid zone is constrained by population density, reduced hybrid fitness, and low dispersal rates. Documenting the formation of a contemporary clinal hybrid zone may provide important insights into the factors that shaped other well-established hybrid zones.

The processes governing soil bacteria biogeography are still not fully understood. It remains unknown how the importance of environmental filtering and dispersal differs between bacterial taxonomic and functional biogeography, and whether their importance is scale-dependent. We sampled soils at 195 plots across the Tibet plateau, with distances among plots ranging from 20 m to 1 550 km. Taxonomic composition of bacterial community was characterized by 16S amplicon sequencing, and functional community composition by qPCR targeting 9 functional groups involved in N dynamics. Twelve climatic and soil characteristics were also measured. Both taxonomic and functional dissimilarities were more related to environmental dissimilarity than geographic distance. Taxonomic dissimilarity was mostly explained by soil pH and organic matter, while functional dissimilarity was mostly linked to moisture, temperature and N, P and C availabilities. The roles of environmental filtering and dispersal were, however, scale-dependent and varied between taxonomic and functional dissimilarities, with distance affecting taxonomic dissimilarity over short distances (<~300 km) and functional dissimilarity over long distances (>~600 km). The importance of different environmental predictors varied across scales more for functional than taxonomic dissimilarity. Our results demonstrate how biodiversity dimension (taxonomic versus functional) and spatial scale strongly influence the conclusions derived from bacterial biogeography studies.

Processes governing genetic diversity and adaptive potential in reef-building corals are of interest both for fundamental evolutionary biology and for reef conservation. Here, we investigated the possibility of “sweepstakes reproductive success” (SRS) in a broadcast spawning coral Acropora hyacinthus at Yap Island, Micronesia. SRS is an extreme yearly variation in the number of surviving offspring among parents. It is predicted to generate genetically differentiated, low genetic diversity recruit cohorts, containing close kin individuals. We have tested these predictions by comparing genetic composition of size classes (adults and juveniles) at several sites on the island of Yap, Micronesia. We did see the genome-wide dip in genetic diversity in juveniles compared to adults at two of the four sites; however, both adults and juveniles varied in genetic diversity across sites, and there was no detectable genetic structure among juveniles, which does not conform to the classical SRS scenario. Yet, we have identified a pair of juvenile siblings at the site where juveniles had the lowest genetic diversity compared to adults, an observation that is hard to explain without invoking SRS. While further support for SRS is needed to fully settle the issue, we show that incorporating SRS into the Indo-West Pacific coral metapopulation adaptation model had surprisingly little effect on mean rates of coral cover decline during warming. Still, SRS notably increases year-to-year variation in coral cover throughout the simulation.

Masting, the synchronous highly variable flowering across years by a population of perennial plants, has been shown to be precipitated by many factors including nitrogen levels, drought conditions, spring and summer temperatures. However, the molecular mechanism leading to the initiation of flowering in masting plants in particular years remains largely unknown, despite the potential impact of climate change on masting phenology. We studied genes controlling flowering in Chionochloa pallens, a strongly masting perennial grass. We used a range of in situ and manipulated plants to obtain leaf samples from tillers (shoots) which subsequently remained vegetative or flowered. Here, we show that a novel orthologue of TERMINAL FLOWER 1 (TFL1; normally a repressor of flowering in other species) promotes the induction of flowering in C. pallens (hence Anti-TFL1), a conclusion supported by structural, functional and expression analyses. Global transcriptomic analysis indicated differential expression of CpTPS1, CpGA20ox1, CpREF6 and CpHDA6, emphasising the role of endogenous cues and epigenetic regulation in terms of responsiveness of plants to initiate flowering. Our molecular-based study has provided insights into the cellular mechanism of flowering in masting plants and will supplement ecological and statistical models to predict how masting will respond to global climate change.

The origin of new genes has long been a central interest of evolutionary biologists. However, their novelty evades reconstruction by the classical tools of evolutionary modeling. This evasion of insight from deep ancestral investigation necessitates intensive study of model species within well-sampled, recently diversified, clades. One such clade is the model genus Neurospora, members of which lack recent gene duplications, yet harbor clusters of lineage-specific genes (LSGs) adjacent to the telomeres. Several Neurospora species are comprehensively characterized organisms apt for studying the evolution of LSGs. Using gene synteny, we documented that 78% of Neurospora LSGs clusters are located in chromosomal regions featuring extensive tracts of non-coding DNA and duplicated genes. Here we report several instances of LSGs that are likely from regional rearrangements and potentially from gene rebirth. To broadly investigate functions of LSGs, we assembled transcriptomics data from 68 experimental data points and identified co-regulatory modules using Weighted Gene Correlation Network Analysis, revealing that LSGs are widely but peripherally involved in known regulatory machinery for diverse functions. The ancestral status of mas-1 and its neighbors was investigated in detail, suggesting that it arose from an ancient lysophospholipase precursor that is ubiquitous in lineages of the Sordariomycetes; mas-1 plays a role in cell-wall integrity and cellular sensitivity to antifungal toxins. Our discoveries illuminate a “rummage region” in the N. crassa genome that enables formation of new genes and functions to arise via gene duplication and relocation, followed by fast mutation and recombination facilitated by tandem repeats and deconstrained non-coding sequences.

While the role of selection in divergence along the speciation continuum is theoretically well understood, defining specific signatures of selection in the genomic landscape of divergence is empirically challenging. Modelling approaches can provide insight into the potential role of selection on the emergence of a heterogenous genomic landscape of divergence. Here, we extend and apply an individual-based approach that simulates the phenotypic and genotypic distributions of two populations under a variety of selection regimes, genotype-phenotype maps, modes of migration, and genotype-environment interactions. We show that genomic islands of high differentiation and genomic valleys of similarity may respectively form under divergent and parallel selection between populations. For both types of between-population selection, negative and positive frequency-dependent selection within populations generated genomic islands of higher magnitude and genomic valleys of similarity respectively. Divergence rates decreased under strong dominance with divergent selection, as well as in models including genotype-environment interactions under parallel selection. For both divergent and parallel selection models, divergence rate was higher under an intermittent migration regime between populations, in contrast to a constant level of migration across generations, despite an equal number of total migrants. We highlight that interpreting a particular evolutionary history from an observed genomic pattern must be done cautiously, as similar patterns may be obtained from different combinations of evolutionary processes. Modelling approaches such as ours provide an opportunity to narrow the potential routes that generate the genomic patterns of specific evolutionary histories.

Adaptive phenotypes are shaped by a combination of genetic and environmental forces, and while the literature is rich with studies focusing on either genetics or environment contributions, those that consider both are rare. Here we utilize the cichlid oral jaw apparatus to fill this knowledge-gap. First, we employed RNA-seq in bony and ligamentous tissues important for jaw opening to identify differentially expressed genes between species and across foraging environments. Our foraging treatments were designed to force animals to employ either suction or biting/scraping, which broadly mimic pelagic or benthic modes of feeding. We found a large number of differentially expressed genes between species, and while we identified relatively few differences between environments, species differences were far more pronounced when reared in the pelagic versus benthic environment. Further, these data carried the signature of genetic assimilation, and implicated cell cycle regulation in shaping the jaw across species and environments. Next, we repeated the foraging experiment and performed ATAC-seq procedures on nuclei harvested from the same tissues. Cross-referencing results from both analyses revealed subsets of genes that were both differentially expressed and differentially accessible in either the pelagic (n=15) or the benthic environment (n=11), as well as loci where differences were robust to foraging environment (n=13). All in all, these data provide novel insights into the epigenetic, genetic, and cellular bases of species- and environment-specific bone shapes, as well as the evolution of phenotypic plasticity in this iconic model system.

Pregnancy, the post-fertilization period when embryos are incubated within the body, is a dynamic multistage process that has convergently evolved in many vertebrates. To increase independence from environmental fluctuations and protect offspring from predation, challenges had to be initially overcome. The most obvious, when considering such an intimate relation between the parent and its semi-allogenic offspring, was the pressing need to dodge immunity-associated embryo rejection. In mammals, immunological tolerance was found to be dependent on the active modulation of the immune system. Even though supporting much of the current knowledge on vertebrate pregnancy, mammals lack extant transitional stages that could help reconstruct the evolutionary pathway of this fascinatingly complex reproduction mode. In this issue of Molecular Ecology, Parker et al. (2022) selected an untraditional model - the seahorse and pipefish family, whose species evolved male pregnancy across an almost continuous gradient of complexity, from external oviparity to internal gestation. By contrasting gene expression profiles of syngnathids with distinct brooding architectures, this study allowed for the observation of subtle evolutionary adaptations, while confirming the existence of remarkable similarities to ‘female’ pregnancy (e.g., the evolution of male pregnancy in pouched species occurred alongside immune downregulation, and inflammation seems vital during early pregnancy stages). In a world where the debate on sex-roles takes centre stage, Parker et al. (2022) appeasing results hint at the fact that the strongly convergent evolution of vertebrate pregnancy was seemingly unaffected by which sex carries the burden of gestation.

Natural hybridisation is now recognised as pervasive in its occurrence across the Tree of Life. Resurgent interest in natural hybridisation fuelled by developments in genomics has led to an improved understanding of the genetic factors that promote or prevent species cross-mating. Despite this body of work overturning many widely held assumptions about the genetic barriers to hybridisation, it is still widely thought that ploidy differences between species will be an absolute barrier to hybridisation and introgression. Here, we revisit this assumption, reviewing findings from surveys of polyploidy and natural hybrids in the wild. In a case study in the British flora, 203 hybrids representing 35% of hybrids with suitable data have formed via cross-ploidy matings, while a wider literature search revealed 48 studies (45 in plants and 3 in animals), where cross-ploidy hybridisation has been confirmed with genetic data. These results show cross-ploidy hybridisation is readily overlooked, and potentially common in some groups. General findings from these studies include strong directionality of hybridisation, with introgression usually towards the higher ploidy parent, and cross-ploidy hybridisation being more likely to involve allopolyploids than autopolyploids. Evidence for adaptive introgression across a ploidy barrier and cases of cross-ploidy hybrid speciation show the potential for important evolutionary outcomes.