Linear infrastructure stands as one of the main culprits of anthropogenically caused biodiversity decline. As it fragments landscapes, it ultimately results in a myriad of direct and indirect ecological consequences for wildlife. As transportation networks will continue to grow under increasing human population growth, biodiversity will continue to decline making the need to understand and mitigate their impact on species an urgent need for conservation worldwide. The implementation of mitigation measures to alleviate the barrier effect produced by linear transport infrastructure on local fauna is not new, and research has shown that their effectiveness has been shown to be influenced by their design, their placement and the biology of the impacted species. Our understanding of their effectiveness in preventing the longer-term impacts of linear transport infrastructure on habitat connectivity via gene flow, however, remains poorly understood. Here, we used a pre- and post-habitat fragmentation genetic dataset collected as part of an extensive Koala Management Program to ask questions about the immediate and predicted longer-term genetic consequences of linear transport infrastructure on the impacted species. Importantly, using forward migration simulations, we show that to preserve connectivity would need to result in around 20% of the population mixing to avoid long-term genetic drift. These results have important consequences for the management of species at the forefront of linear infrastructure. In particular, the study shows the importance of considering gene flow in our assessment of the effectiveness of fauna crossings.
Reproductive phenotypes are shaped by genetic, physiological and environmental variation that an organism experiences during ontogeny. Steroid hormones play an integrative role in this process through both genomic and non-genomic pathways. Differences in steroid hormone metabolism may be rooted in genomic variation. Here we evaluate the influence of supergene variants underlying alternative reproductive tactics on sex steroid metabolism during ontogeny in ruffs (Calidris pugnax). Adult ruff males exhibit three male mating morphs called Independents, Faeders and Satellites, that differ prominently in circulating androgen (testosterone and androstenedione) concentrations. Across morphs and sexes chicks showed similar mean androgen concentrations during ontogenetic development. However, variances in circulating androgens showed the same pattern as corresponding variances previously observed in adults. HSD17B2 had been previously identified as a key gene for mediating differences in androgen levels between morphs as it encodes the enzyme that converts testosterone to androstenedione and is located within the supergene. Observed HSD17B2 expression in embryonic brain tissue was consistent with predictions based on genetic and endocrine differences. Taken together, the observed differences in circulating androgen concentrations and gene expression point to testosterone synthesis as a key mechanism that shapes developmental trajectories and differences in brain organization among morphs.
By evaluating genetic variation across the entire genome, one can address existing questions in a novel way while new can be asked. Such questions include how different local environments influence both adaptive and neutral genomic variation within and among populations, providing insights not only into local adaptation of natural populations, but also into their responses to global change and the exploitation-induced evolution. Here, under a seascape genomic approach, ddRAD genomic data were used along with environmental information to uncover the underlying processes (migration, selection) shaping European sardines (Sardina pilchardus) of the Western Mediterranean and adjacent Atlantic waters. This information can be relevant to the (re)definition of fishery stocks, and their short-term adaptive potential. We found that studied sardine samples form two clusters, detected using both neutral and adaptive (outlier) loci suggesting that natural selection and local adaptation play a key role in driving genetic change among the Atlantic and the Mediterranean sardines. Temperature and especially the trend in the number of days with sea surface temperature (SST) above 19oC was crucial at all levels of population structuring with implications on species’ key biological processes, especially reproduction. Our findings provide evidence for a dynamic equilibrium where population structure is maintained by physical and biological factors under the opposing influences of migration and selection. Given its dynamic nature, such a system postulates a continuous monitoring under a seascape genomic approach that can benefit by incorporating a temporal as well as a more detailed spatial dimension.
Anthropogenic biological invasions represent major concerns but enable us to investigate rapid evolutionary changes and adaptation to novel environments. The goldfish Carassius auratus with sexual diploids and asexual triploids coexisting in natural waters, is one of the most widespread invasive fishes in Tibet, providing an ideal model to study evolutionary processes during invasion in different reproductive forms from the same vertebrate. Here, using whole-genome resequencing data of 151 C. auratus individuals from invasive and native ranges, we found different patterns of genomic responses between diploid and triploid populations during their invasion to Tibet. For diploids, although invasive individuals derived from two different genetically distinct sources and had a relative higher diversity (π) at the population level, their individual genetic diversity (genome-wide observed heterozygosity) was significantly lower (21.4%) than that of source individuals. Population structure analysis revealed that the invasive individuals formed a specific genetic cluster distinct from the source populations. Runs of homozygosity analysis showed low inbreeding only in invasive individuals, and only the invasive population experienced a recent decline in effective population size reflecting founder events. For triploids, however, invasive populations showed no loss of individual genetic diversity and no genetic differentiation relative to source populations. Regions of putative selective sweeps between invasive and source populations of diploids mainly involved genes associated with mannosidase activity and embryo development. Our results suggest invasive diploids deriving from distinct sources still lost individual genetic diversity resulting from recent inbreeding and founder events and selective sweeps, and invasive triploids experienced no genetic change owing to their reproduction mode of gynogenesis that precludes inbreeding and founder effects and may make them more powerful invaders.
Recombination generates new combination of alleles, whereby it maintains haplotype diversity and enhances the efficacy of selection. Despite the apparent stasis in positioning recombination events in birds, recombination rates differ widely across the genome and within species. The causes of recombination rate variation and its evolutionary impact on natural populations remain poorly understood. We used whole-genome resequencing data of 167 individuals of the Eurasian blackcap (Sylvia atricapilla) to characterise the historical recombination landscape variation at broad and fine scales among populations with distinct migratory phenotypes. We additionally evaluated the interplay between recombination rates with patterns of genetic diversity, population divergence (based on Fst and dxy), and potential signs of selection. Our comparative analyses revealed: i) Lower divergence of recombination maps at the broad scale and higher variability at fine scales. Resident island populations showed higher variability in recombination patterns among them and with continental populations. Recombination rates were more conserved in continental populations regardless of the migratory phenotype. ii) The degree of divergence between recombination maps correlated with population differentiation. It could also recapitulate population-specific demographic history and genetic structure. iii) Recombination rates correlated negatively with Fst and positively with nucleotide diversity and dxy, suggesting that recombination may reduce the effect of linked selection over the loss of neutral diversity. We identified chromosomal regions with potential signs of linked selection. This study evidences that recombination is a variable trait that shapes the diversity and evolution of population differentiation in the blackcap.
Ecological or reproductive barriers can maintain species by preventing introgression in closely related taxa when their distributions overlap. In sympatry, sister-taxa may have greater genetic divergence than comparing the sister-taxa in allopatric parts of their range. When analyzing populations within a species, this may translate to greater genetic divergence between sympatry and allopatry. This genetic differentiation can be caused by either genetic drift or natural selection, depending on the evolutionary history of secondary contact. To identify a selective process, it is critical to find genes responsible for maintaining species barriers in sympatry. Here, we examined the role of natural selection in genetic differentiation within two recently diverged rockfish species, Sebastes diaconus and Sebastes mystinus. These species overlap along over 400 km of coastline in the eastern Pacific, with no evidence of hybridization. We found evidence of geographic genetic differentiation across a large span of the S. diaconus range, but not within S. mystinus. For both species, we identified outlier loci associated with regions of the genome under directional selection in allopatric versus sympatric populations. We also found signals of directional selection in shared genomic regions of both species, suggesting the evolutionary process of reinforcement maintained species boundaries once the two species were in secondary contact.
Parasitoid wasps are major causes of mortality of many species, and therefore traits related to host immune defence are usually favoured by natural selection. One powerful approach to detect functionally important genes under natural selection is through the analysis of directional selection acting upon protein-coding gene sequences across different species. Here, we investigated patterns of positive selection across three closely related leaf beetle species with different immune defence capacity against a shared parasitoid wasp using a Bayesian approach for the McDonald–Kreitman test. Focusing on single-copy orthologs for Coleoptera, as well as on candidate immune related genes, we detected species-specific positive selection on coding regions in each of the closely related Galerucella beetle species. Results indicated that more immune genes had experienced positive selection in the species with the greatest immunocompetence (G. pusilla) against parasitoid wasps, while almost no immune genes were under positive selection in the species with the least immunocompetence (G. calmariensis).
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.
Host-parasite interactions can cause strong demographic fluctuations accompanied by selective sweeps of resistance/infectivity alleles. Both demographic bottlenecks and frequent sweeps are expected to reduce the amount of segregating genetic variation and therefore might constrain adaption during coevolution. Recent studies, however, suggest that the interaction of demographic and selective processes is a key component of coevolutionary dynamics and may rather positively affect levels of genetic diversity available for adaptation. Here, we provide direct experimental testing of this hypothesis by disentangling the effect of demography, selection, and of their interaction in an experimental host-parasite system. We grew 12 populations of unicellular algae (Chlorella variabilis) that experienced either growth followed by constant population sizes (3 populations), demographic fluctuations (3 populations), selection induced by exposure to a virus (3 populations), or demographic fluctuations together with virus-induced selection (3 populations). After 50 days, we conducted whole-genome sequencing of each algal population. We observed more genetic diversity in populations that jointly experienced selection and demographic fluctuations than in populations where these processes were experimentally separated. In addition, in those 3 populations that jointly experienced selection and demographic fluctuations, experimentally measured diversity exceeds expected values of diversity that account for the cultures’ population sizes. Our results suggest that eco-evolutionary feedbacks can positively affect genetic diversity and provide the necessary empirical measures to guide further improvements of theoretical models of adaptation during host-parasite coevolution.
Landscape genetics is increasingly transitioning away from microsatellites, with Single Nucleotide Polymorphisms (SNPs) providing increased resolution for detecting patterns of spatial-genetic structure. This is particularly pertinent for research in arid-zone mammals due to challenges associated with unique life history traits, boom-bust population dynamics and long-distance dispersal capacities. Here, we provide a case study assessing the performance of SNPs versus microsatellites in evaluating three explicit landscape genetic hypotheses (isolation-by-distance, isolation-by-barrier, and isolation-by-resistance) in a suite of small, arid-zone mammals in the Pilbara region of Western Australia. Using clustering algorithms, Mantel tests, and linear mixed effects models, we compare functional connectivity between genetic marker types and across species, including one marsupial, Ningaui timealeyi, and two native rodents, Pseudomys chapmani and P. hermannsburgensis. SNPs resolved subtle genetic structuring not detected by microsatellites, particularly for N. timealeyi where two genetic clusters were identified. Furthermore, stronger signatures of isolation-by-distance and isolation-by-resistance were detected when using SNPs, and model selection based on SNPs tended to identify more complex resistance surfaces (i.e., composite surfaces of multiple environmental layers) in the best-performing models. While we found limited evidence for physical barriers to dispersal across the Pilbara for all species, we found that topography, substrate, and soil moisture were the main environmental drivers shaping functional connectivity. Our study demonstrates that new analytical and genetic tools can provide novel ecological insights into arid landscapes, with potential application to conservation management through identifying dispersal corridors to mediate the impacts of ongoing habitat fragmentation in the region.
Understanding the population structure of a species is important to accurately assess its conservation status and manage the risk of local extinction. The Bull Shark (Carcharhinus leucas) faces varying levels of exploitation around the world due to its coastal distribution. Information regarding population connectivity is crucial to evaluate its conservation status and local fishing impacts. In this study, we sampled 922 putative Bull Sharks from 19 locations in the first global assessment of population structure of this cosmopolitan species. Using a recently developed DNA-capture approach (DArTcap), samples were genotyped for 3,400 nuclear markers. Additionally, full mitochondrial genomes of 384 Indo-Pacific samples were sequenced. Reproductive isolation was found between and across ocean basins (eastern Pacific, western Atlantic, eastern Atlantic, Indo-West Pacific) with distinct island populations in Japan and Fiji. Bull Sharks appear to maintain reproductive connectivity using shallow coastal waters as dispersal corridors, whereas large oceanic distances and historical land-bridges act as barriers. Females tend to return to the same area for reproduction, making them more susceptible to local threats and an important focus for management actions. Given these behaviours, the exploitation of Bull Sharks from insular populations, such as Japan and Fiji, may instigate local decline that cannot readily be replenished by immigration, which can in turn affect ecosystem dynamics and functions. These data also supported the development of a genetic panel to ascertain the population of origin, which will be useful in monitoring the trade of fisheries products and assessing population-level impacts of this harvest.
An exhaustive assessment of biodiversity is a major challenge of ecological research, and molecular approaches such as the metabarcoding of environmental DNA are boosting our ability to perform biodiversity inventories. Are we actually able to assess the whole community, to unravel the intricate interactions between organisms and the impacts of global changes on the different trophic levels? The majority of metabarcoding papers published in the last years used just one or two markers and analyzed a limited number of taxonomic groups. Nevertheless, approaches are emerging that might allow “all-taxa biological inventories”. Exhaustive biodiversity assessments can be attempted by combining a large number of specific primers, by exploiting the power of universal primers, or by combining specific and universal primers to obtain good information on key taxa while limiting the overlooked biodiversity. Multiplexes of primers and shotgun sequencing may provide a better coverage of biodiversity compared to standard metabarcoding, but still require major methodological advances. We identify the strengths and limitations of different approaches, and suggest new development lines that might improve broad scale biodiversity analyses in the near future.
Anthropogenic changes have altered the historical distributions of many North American taxa. As environments shift, ecological and evolutionary processes can combine in complex ways to either stimulate or inhibit range expansion. Here we examine the role of evolution in a rapid range expansion whose ecological context has been well-documented, Anna’s Hummingbird (Calypte anna). Previous work suggests that the C. anna range expansion is the result of an ecological release facilitated by human-mediated environmental changes, where access to new food sources have allowed further filling of the abiotic niche. We examine the role of gene flow and adaptation during range expansion from their native California north into Canada and east into New Mexico and Texas, USA. Using low coverage whole genome sequencing we found high genetic diversity, low divergence, and little evidence of selection on the northern and eastern expansion fronts. Additionally, there are few (if any) limits to gene flow across the native and expanded range. The lack of selective signals between core and expanded ranges could reflect i) an absence of novel selection pressure in the extended range (supporting the ecological release hypothesis), ii) swamping of adaptive variation due to high gene flow, or iii) limitations of genome scans for detecting small shifts in allele frequencies across many loci. Nevertheless, our results provide an example where strong selection is not apparent during a rapid, contemporary range shift.
The mutualistic lifestyle of pollinating fig wasps and fig trees provides an excellent model for studying ecological and adaptive evolution issues. Transposable elements (TEs), as an important component of the genomes, are powerful driver for organisms to adapt to environment. Here, the genomic TEs of six pollinating fig wasps and five non-pollinating fig wasps were analyzed in the characteristics of composition and their effects on genome size, the historical burst patterns and their association with effective population size and paleoclimate changes, to infer the role of TEs in environmental adaptation in fig wasps. Compared with non-pollinators, pollinators’ TEs showed a significantly different burst state with less types and amount, shorter lengths, and lower contents in the genomes. The recent smaller effective population size and contractive demography failed to cause pollinators to accumulate more TEs, while the large number of TEs accumulated in non-pollinators positively correlated with their population expansion. The major TEs burst peaks in the history of pollinators highly overlapped with the warmer times in the Coolhouse in geological history. TEs located in the major peak period were mostly inserted near genes related to environment information processing such as Circadian entrainment pathway, and might act as CRMs (cis-regulatory modules) to regulate the conjunctive genes in response to paleoclimate changes in pollinators. These results revealed the molecular basis of the fig wasp’s response to changes in the syconia microenvironment and paleoclimate macroenvironment from the perspective of genomic TEs.
Genomes retain evidence of the demographic history and evolutionary forces that have shaped populations. Across island systems, contemporary patterns of genetic diversity reflect complex population demography, including colonisation events, bottlenecks, gene flow and genetic drift. Here, we investigate whether island founder events have prolonged effects on genome-wide diversity and runs of homozygosity (ROH) distributions, using whole genome resequencing from six populations across three archipelagos of Berthelot’s pipit (Anthus berthelotii) - a passerine which has undergone island speciation relatively recently. Pairwise sequential Markovian coalescent (PSMC) analyses estimated divergence from its sister species approximately two million years ago. Results indicate that all Berthelot’s pipit populations had shared ancestry until approximately 50,000 years ago, when the Madeiran archipelago populations were founded, while the Selvagens were colonised within the last 8,000 years. We identify extensive long ROH (>1 Mb) in genomes in the most recently colonised populations of Madeira and Selvagens which have experienced sequential island founder events and population crashes. Population expansion within the last 100 years may have eroded long ROH in the Madeiran archipelago, resulting in a prevalence of short ROH (<1 Mb). Extensive long and short ROH in the Selvagens reflects strong recent inbreeding, small contemporary effective population size and past bottleneck effects, with as much as 37.7% of the autosomes comprised of ROH >250 kb in length. These findings highlight the importance of demographic history, as well as selection and genetic drift, in shaping contemporary patterns of genomic diversity across diverging populations.
Skin microbiomes provide vital functions, yet knowledge about their species assemblages is limited - especially for non-model organisms. In this study, we conducted in situ manipulations and repeated sampling on wild-caught individuals of Rutilus rutilus. Treatments included translocation between fresh and brackish water habitats to investigate the role of environment; community rebooting by disinfection to infer host-microbe interactions; and housing in pairs to study the role of inter-host dispersal for the structure of microbiomes colonizing animals. Results revealed that fish skin microbiomes were biodiversity hotspots with highly dynamic composition that were distinct from bacterioplankton communities. External environmental conditions and individual-specific factors jointly determined the colonization-extinction dynamics, whereas inter-host dispersal had negligible effects. The dynamics of the microbiome composition was seemingly non-affected by reboot treatment, pointing to high resilience to disturbance in these microbial communities. Together, the manipulations demonstrate that host individual characteristics and environment interactively shapes the skin microbiome of fish. The results emphasize the role of inter-individual variability for the unexplained variation found in many host-microbiome systems, although the mechanistic underpinnings remain to be identified.
Wolbachia are among the most prevalent and widespread endosymbiotic bacteria on earth. Wolbachia’s success in infecting an enormous number of arthropod species is attributed to two features: the range of phenotypes they induce in their hosts, and their ability to switch between host species. Whilst much progress has been made in elucidating their induced phenotypes, our understanding of Wolbachia host shifting is still very limited: we lack answers to even fundamental questions concerning Wolbachia’s routes of transfer and the importance of factors influencing host shifts. Here, we investigate the diversity and host-shift patterns of Wolbachia in scale insects, a group of arthropods with intimate associations with other insects that make them well-suited to studying host shifts. Using Illumina multi-target amplicon sequencing of Wolbachia-infected scale insects and their direct associates we determined the identity of all Wolbachia strains. We then fitted a Generalised Additive Mixed Model (GAMM) to our data to estimate the influence of host phylogeny and the geographic distribution on Wolbachia strain sharing among scale insect species. The model predicts no significant contribution of host geography but strong effects of host phylogeny, with high rates of Wolbachia sharing among closely related species and a sudden drop-off in sharing with increasing phylogenetic distance. We also detected the same Wolbachia strain in scale insects and several intimately associated species (ants, wasps, beetles, and flies). This indicates putative host shifts and potential routes of transfers via these associates and highlights the importance of ecological connectivity in Wolbachia host-shifting.
Quantifying genetic structure and levels of genetic variation are fundamentally important to predicting the ability of populations to persist in human-altered landscapes and adapt to future environmental changes. Genetic structure reflects the dispersal of individuals over generations, which can be mediated by species-level traits or environmental factors. Dispersal distances are commonly positively associated with body size and negatively associated with the amount of degraded habitat between sites, motivating investigation of these potential drivers of dispersal concomitantly. We quantified genetic structure and genetic variability within populations of ten bee species in the tribe Euglossini across fragmented landscapes. We genotyped bees at thousands of SNP loci and tested the following predictions: (1) larger species disperse farther; (2) species with greater resource specialization disperse farther; (3) deforested areas restrict dispersal; and (4) sites surrounded by more intact habitat have higher genetic diversity. Body size was a strong predictor of genetic structure, but, surprisingly, larger species showed higher genetic structure than smaller species. The way that deforestation affected dispersal varied with body size, such that larger species dispersed less far in areas with more forest. There was no effect of geographic distance on dispersal, and sites with more intact habitat had higher genetic diversity. These results challenge the dominant paradigm that individuals of larger species disperse farther, motivating further work into ecological drivers of dispersal for bees.