Understanding how eco-evolutionary processes shape genetic variation and persistence in marine species with highly variable recruitment dynamics and dispersal potential remains a fundamental challenge, particularly when considering the interplay between gene flow and local adaptation. Here, we employed a seascape genomics approach to investigate population connectivity and local adaptation in Australasian snapper (Chrysophrys auratus, Sparidae) along 1500 km of the environmentally heterogeneous southern Australian coastline. Using genome-wide SNPs, we identified distinct eastern and western regional populations aligned with known biogeographical regions. Genotype-environment association analyses revealed 855 candidate adaptive loci associated with environmental variation, including temperature, salinity and primary productivity. Connectivity analyses using neutral markers indicated high gene flow within both eastern and western regions, while candidate adaptive loci revealed substantially reduced connectivity, especially for Northern Spencer Gulf and West Coast populations. This contrast implies a decoupling of demographic and adaptive connectivity, in which strong environmental gradients appear to reduce the effective exchange of adaptive variation despite high overall connectivity. Our results support contingent migration as a potential mechanism modulating the balance between local adaptation and gene flow in this economically and ecologically important marine species. These findings might also have implications for regional management of other coastal fisheries that are experiencing substantial declines. As climate change alters coastal marine environments around the world, the dynamics of local recruitment, site fidelity and local adaptation are expected to change. This highlights the importance of integrating knowledge about eco-evolutionary processes into marine resource management, fisheries stock assessment, and restocking and stock enhancement activities.
The persistence of many threatened species depends on isolated habitat patches such as conservation parks, fenced reserves, and islands. While these 'conservation arks' provide refuge from many contemporary threats, they can also pose risks of genetic diversity loss and inbreeding depression, further exacerbating extinction risk. A pertinent example is the Kangaroo Island koala population in South Australia that originated from a few translocated founding individuals in the 1920s but now sustains a large population with a low prevalence of infectious disease. We investigated the extent and consequences of founder effects on genomic diversity, inbreeding, and adaptive potential in Kangaroo Island koalas by comparing them with mainland Australian populations using high-coverage whole genomes. Our findings support sharp, recent declines in effective population sizes (Ne) in both mainland and Kangaroo Island populations. However, Kangaroo Island koalas had much lower individual and population-level diversity. Together with longer and more numerous runs of homozygosity and an increased proportion of homozygous genetic load, these results support the hypothesis that a severe bottleneck has contributed to inbreeding and maladaptation in Kangaroo Island koalas. While Kangaroo Island has the potential to conserve a viable population of koalas, we recommend genetic rescue to restore diversity and mitigate inbreeding depression in this isolated population. Our results emphasise the need for longitudinal genomic monitoring and genetic management to maintain long-term viability and resilience in potential conservation arks. Understanding the demographic history of such populations will help inform future conservation aimed at preventing genetic erosion and preserving biodiversity.
The International Union for Conservation of Nature (IUCN) Green Status of Species (GSS), introduced in 2021, is a global standard of measurement used to assess the level to which a species has recovered (i.e., is viable and providing its ecological function across its entire range). It is also used to evaluate how a species has responded to past conservation actions and the expected conservation gains and recovery potential it would receive in the short- and long-term future. Preliminary application of the GSS method has relied on expert knowledge from individuals or small groups of specialists. However, more accurate and reliable results are likely to be produced by formally eliciting individual judgments from a diverse range of experts, followed by discussion, reevaluation, and synthesis of these judgments. We developed a method in which 2 structured expert elicitation workshops are used to conduct GSS assessments and applied this method to 8 Australian freshwater fish species from the Murray-Darling Basin. We integrated the investigate, discuss, evaluate, aggregate protocol into the GSS methods; experts assessed the species' IUCN Green Score (percent recovery) in the current state and for 5 other scenarios in the past and future with and without conservation. Four GSS conservation impact metrics were calculated based on the averages of expert judgments. Experts forecasted that impact in the short-term would be minimal (i.e., conservation gain metric = zero or low) for 5 of the 8 species because targeted and maintained conservation actions are often lacking. In contrast, experts indicated long-term recovery potential would be considerably higher if implementation of appropriate recovery activities could be sustained (all 8 species had medium or high recovery potential). We concluded that the GSS is well suited to a modified workshop approach because it aims to reduce biases associated with expert judgments and encourages valuable knowledge sharing among experts.
Genetic rescue is a conservation management strategy that reduces the negative effects of genetic drift and inbreeding in small and isolated populations. However, such populations might already be vulnerable to random fluctuations in growth rates (demographic stochasticity). Therefore, the success of genetic rescue depends not only on the genetic composition of the source and target populations but also on the emergent outcome of interacting demographic processes and other stochastic events. Developing predictive models that account for feedback between demographic and genetic processes ('demo-genetic feedback') is therefore necessary to guide the implementation of genetic rescue to minimize the risk of extinction of threatened populations. Here, we explain how the mutual reinforcement of genetic drift, inbreeding, and demographic stochasticity increases extinction risk in small populations. We then describe how these processes can be modelled by parameterizing underlying mechanisms, including deleterious mutations with partial dominance and demographic rates with variances that increase as abundance declines. We combine our suggestions of model parameterization with a comparison of the relevant capability and flexibility of five open-source programs designed for building genetically explicit, individual-based simulations. Using one of the programs, we provide a heuristic model to demonstrate that simulated genetic rescue can delay extinction of small virtual populations that would otherwise be exposed to greater extinction risk due to demo-genetic feedback. We then use a case study of threatened Australian marsupials to demonstrate that published genetic data can be used in one or all stages of model development and application, including parameterization, calibration, and validation. We highlight that genetic rescue can be simulated with either virtual or empirical sequence variation (or a hybrid approach) and suggest that model-based decision-making should be informed by ranking the sensitivity of predicted probability/time to extinction to variation in model parameters (e.g., translocation size, frequency, source populations) among different genetic-rescue scenarios.
Freshwater ecosystems and their biota are under increasing pressure from anthropogenic stressors. In response to declining fish stocks, hatchery and stocking programmes are widely implemented as core components of restoration and management strategies, with positive outcomes for some wild populations. Despite this, stocking remains contentious due to potential genetic and ecological risks to wild populations. Monitoring and evaluation of stocking outcomes are critical to ensuring the long-term sustainability of wild populations, but identification of stocked individuals post-release remains a key challenge, particularly for mobile species. In this study, we combined otolith (natal origin and age) and genomic data to identify stocked individuals and evaluate the genetic implications of stocking for a culturally and socioeconomically important and mobile freshwater fish, golden perch Macquaria ambigua (family: Percichthyidae), across Australia's Murray-Darling Basin (MDB). We also generated a chromosome-level genome assembly. Many close kin were detected across the MDB, increasing in prevalence over recent decades and mostly of hatchery origin. Rivers with many close kin were associated with low effective population sizes (Ne < 100). Genetic signatures of stocking varied according to local context, being most pronounced in but not restricted to rivers considered functionally isolated for management purposes. Where fish are stocked into rivers that are part of the connected metapopulation, there is scope to modify current stocking practices to avoid over-representation of related stocked individuals. Increased focus on the genetic diversity of stocked fish is likely to promote the long-term persistence of golden perch in the wild.
Marine ecosystems are ideal for studying evolutionary adaptations involved in lineage diversification due to few physical barriers and reduced opportunities for strict allopatry compared to terrestrial ecosystems. Cetaceans (whales, dolphins, and porpoises) are a diverse group of mammals that successfully adapted to various habitats within the aquatic environment around 50 million years ago. While the overall adaptive transition from terrestrial to fully aquatic species is relatively well understood, the radiation of modern whales is still unclear. Here high-quality genomes derived from previously published data were used to identify genomic regions that potentially underpinned the diversification of baleen whales (Balaenopteridae). A robust molecular phylogeny was reconstructed based on 10,159 single copy and complete genes for eight mysticetes, seven odontocetes and two cetacean outgroups. Analysis of positive selection across 3,150 genes revealed that balaenopterids have undergone numerous idiosyncratic and convergent genomic variations that may explain their diversification. Genes associated with aging, survival and homeostasis were enriched in all species. Additionally, positive selection on genes involved in the immune system were disclosed for the two largest species, blue and fin whales. Such genes can potentially be ascribed to their morphological evolution, allowing them to attain greater length and increased cell number. Further evidence is presented about gene regions that might have contributed to the extensive anatomical changes shown by cetaceans, including adaptation to distinct environments and diets. This study contributes to our understanding of the genomic basis of diversification in baleen whales and the molecular changes linked to their adaptive radiation, thereby enhancing our understanding of cetacean evolution.
Marine ecosystems are highly dynamic, and their connectivity is affected by a complex range of biological, spatial, and oceanographic factors. Incorporating connectivity as a factor in the planning and management of marine protected areas (MPAs) is important yet challenging. Here, we implemented a novel integrative framework that uses intraspecific genetic and genomic data for multiple marine species to characterise connectivity across a recently established South Australian MPA network. We generated connectivity networks, estimated cross-species concordance of connectivity patterns, and tested the impact of key spatial and oceanographic factors on each species. Connectivity patterns varied markedly among species, but were most correlated among those with similar dispersal strategies. Ordination analyses revealed significant associations with both waterway distances and oceanographic advection models. Notably, waterway distances provided better predictive power in all-species combined analyses. We extended the practical relevance of our findings by employing spatial prioritisation with Marxan, using node values derived from both genetic and geographic connectivity networks. This allowed the identification of several priority areas for conservation, and substantiated the initial decision to employ spatial distance as a proxy for biological connectivity for the design of the South Australian marine park network. Our study establishes a baseline for connectivity monitoring in South Australian MPAs, and provides guidelines for adapting this framework to protected networks elsewhere in the world.
Download This Paper Open PDF in Browser Add Paper to My Library Share: Permalink Using these links will ensure access to this page indefinitely Copy URL Copy DOI
Obtaining reliable estimates of the effective number of breeders (Nb) and generational effective population size (Ne) for fishery-important species is challenging because they are often iteroparous and highly abundant, which can lead to bias and imprecision. However, recent advances in understanding of these parameters, as well as the development of bias correction methods, have improved the capacity to generate reliable estimates. We utilized samples of both single-cohort young of the year and mixed-age adults from two geographically and genetically isolated stocks of the Australasian snapper (Chrysophrys auratus) to investigate the feasibility of generating reliable Nb and Ne estimates for a fishery species. Snapper is an abundant, iteroparous broadcast spawning teleost that is heavily exploited by recreational and commercial fisheries. Employing neutral genome-wide SNPs and the linkage-disequilibrium method, we determined that the most reliable Nb and Ne estimates could be derived by genotyping at least 200 individuals from a single cohort. Although our estimates made from the mixed-age adult samples were generally lower and less precise than those based on a single cohort, they still proved useful for understanding relative differences in genetic effective size between stocks. The correction formulas applied to adjust for biases due to physical linkage of loci and age structure resulted in substantial upward modifications of our estimates, demonstrating the importance of applying these bias corrections. Our findings provide important guidelines for estimating Nb and Ne for iteroparous species with large populations. This work also highlights the utility of samples originally collected for stock structure and stock assessment work for investigating genetic effective size in fishery-important species.
Blue whales (Balaenoptera musculus) are the largest living animal and, like other baleen whales, became endangered due to whaling. Here, we used population genomics to infer the number, distribution and other characteristics of subspecies and populations. We used the largest DNA dataset in blue whales, both in terms of genomic markers (16,661 SNPs and mtDNA) and geographic coverage (n = 276 for SNPs; n = 531 for mtDNA). We found greatest divergence among the eastern Pacific, Indo-western Pacific and Antarctic blue whales. There were indications that natural selection in different environments promoted divergence among these groupings. Within these regions, there was divergence between the eastern North and eastern South Pacific, and among the eastern Indian Ocean, the western South Pacific and the northern Indian Ocean. There was no divergence within the Antarctic. These findings are consistent with the current classification of Antarctic and Indo-western Pacific blue whales in the Southern Hemisphere as different subspecies but call into question the subspecies taxonomy of eastern Pacific blue whales. The study shows that opposite breeding seasons on either side of the equator do not necessarily inhibit connectivity across the equator, and reinforces that population structure needs to be well understood to conserve the diversity within species. Blue whales are the largest living animal and became endangered due to whaling. We found three major groupings of blue whales using high-resolution population genomics: the eastern Pacific, Indo-western Pacific, and Antarctic blue whales. Within these groupings, there was divergence between the eastern North and eastern South Pacific; between the eastern Indian Ocean, the western South Pacific, and the northern Indian Ocean; and no divergence within the Antarctic. The study reinforces that population structure needs to be well understood to conserve the diversity within species. image
Genomic vulnerability is a measure of how much evolutionary change is required for a population to maintain optimal genotype-environment associations under projected climates. Aquatic species, and in particular migratory ectotherms, are largely underrepresented in studies of genomic vulnerability. Such species might be well equipped for tracking suitable habitat and spreading diversity that could promote adaptation to future climates. We characterised range-wide genomic diversity and genomic vulnerability in the migratory and fisheries-important golden perch (Macquaria ambigua) from Australia's expansive Murray-Darling Basin (MDB). The MDB has a steep hydroclimatic gradient and is one of the world's most variable regions in terms of climate and streamflow. Golden perch are threatened by fragmentation and obstruction of waterways, alteration of flow regimes, and a progressively hotter and drying climate. We gathered a genomic dataset of 1049 individuals from 186 MDB localities. Despite high range-wide gene flow, golden perch in the warmer, northern catchments had higher predicted vulnerability than those in the cooler, southern catchments. A new cross-validation approach showed that these predictions were insensitive to the exclusion of individual catchments. The results raise concern for populations at warm range edges, which may already be close to their thermal limits. However, a population with functional variants beneficial for climate adaptation found in the most arid and hydrologically variable catchment was predicted to be less vulnerable. Native fish management plans, such as captive breeding and stocking, should consider spatial variation in genomic vulnerability to improve conservation outcomes under climate change, even for dispersive species with high connectivity.
Even before genome sequencing, genetic resources have supported species management and breeding programs. Current technologies, such as long-read sequencing, resolve complex genomic regions, like those rich in repeats or high in GC content. Improved genome contiguity enhances accuracy in identifying structural variants (SVs) and transposable elements (TEs). We present an improved genome assembly and SV catalogue for the Australasian snapper (Chrysophrys auratus). The new assembly is more contiguous, allowing for putative identification of 14 centromeres and transfer of 26,115 gene annotations from yellowfin seabream. Compared to the previous assembly, 35,000 additional SVs, including larger and more complex rearrangements, were annotated. SVs and TEs exhibit a distribution pattern skewed towards chromosome ends, likely influenced by recombination. Some SVs overlap with growth-related genes, underscoring their significance. This upgraded genome serves as a foundation for studying natural and artificial selection, offers a reference for related species, and sheds light on genome dynamics shaped by evolution.
Anthropogenic climate change is forecast to drive regional climate disruption and instability across the globe. These impacts are likely to be exacerbated within biodiversity hotspots, both due to the greater potential for species loss but also to the possibility that endemic lineages might not have experienced significant climatic variation in the past, limiting their evolutionary potential to respond to rapid climate change. We assessed the role of climatic stability on the accumulation and persistence of lineages in an obligate freshwater fish group endemic to the southwest Western Australia (SWWA) biodiversity hotspot. Using 19,426 genomic (ddRAD-seq) markers and species distribution modelling, we explored the phylogeographic history of western (Nannoperca vittata) and little (Nannoperca pygmaea) pygmy perches, assessing population divergence and phylogenetic relationships, delimiting species and estimating changes in species distributions from the Pliocene to 2100. We identified two deep phylogroups comprising three divergent clusters, which showed no historical connectivity since the Pliocene. We conservatively suggest these represent three isolated species with additional intraspecific structure within one widespread species. All lineages showed long-term patterns of isolation and persistence owing to climatic stability but with significant range contractions likely under future climate change. Our results highlighted the role of climatic stability in allowing the persistence of isolated lineages in the SWWA. This biodiversity hotspot is under compounding threat from ongoing climate change and habitat modification, which may further threaten previously undetected cryptic diversity across the region.
Genetic rescue is now a serious management consideration for protecting small and isolated populations from the negative effects of inbreeding and genetic drift on genetic diversity and population viability. However, such populations might be already vulnerable to random fluctuations in growth rates (demographic stochasticity). Therefore, the success of genetic rescue depends not only on the genetic composition of the source and target populations, but also on the emergent outcome of interacting demographic processes and other stochastic events. Developing predictive models that account for feedback between demographic and genetic processes ('demo-genetic feedback') is therefore necessary to guide genetic-rescue interventions that potentially minimise the risk of extinction of threatened populations. We review the available software and explore how they could be used to develop practical simulations that incorporate demo-genetic feedback to plan and implement scenarios of genetic rescue. We then present a summary of a literature search of available genetic data using Australian threatened marsupials as a case study. We conclude with a guided approach for making model-based decisions on implementing genetic rescue.
Understanding species capacities to adjust to shifting thermal environments is crucial amidst current climate-mediated ocean warming. Fish populations displaying high thermal plasticity can undergo molecular, metabolic, and mitochondrial modifications in response to heat stress. Under the context of heat stress, such acclimation provides a means to maintain normal biological functions through alteration of thermal performance and provides a model to dictate which species will persist when this stress becomes prolonged. Here we combine measures of mitochondrial physiology (using a novel fluorescent technique) and gene expression analyses to investigate thermal resilience and acclimation capacity of two closely related endemic triplefin species, the intertidal common triplefin (Forsterygion lapillum) and the estuarine triplefin (F. nigripenne). Triplefins are an ideal evolutionary model to explore the molecular basis of thermal resilience. Both species evolved in thermally variable environments and are thus predicted to display resistance to heat stress. We observed enhanced mitochondrial function at higher temperatures, although only ATP production was significantly enhanced for both species. Different gene expression profiles were detected between warm acclimated and control fish, with high interspecific variation in acclimatory responses across brain transcriptomes. Differential gene expression and gene ontology highlighted an induction of stress response pathways and oxidoreductase activity in warm acclimated tissues, alongside a rearrangement of metabolic functions facilitating increased carbohydrate metabolism. Our findings indicate thermal acclimation potential in both species, with plasticity in mitochondrial performance enhancing upper thermal tolerance and transcriptional evidence of thermal compensation and homeostatic adjustments under warming conditions. Overall, these results demonstrate robust mechanisms of resilience in coastal fish species that have evolved under climatic variable conditions and provide a new methodological approach for future thermal studies.
Abstract Collaborative approaches to conservation management are critical to respond to the ongoing biodiversity crisis. However, local community involvement in many conservation actions is lacking, especially within translocation and reintroduction programs. Similarly, rapid integration of genetic information into collaborative programs with local communities is rarely conducted. Here, we describe a community‐based and collaborative reintroduction program for a threatened Australian freshwater fish, the southern pygmy perch (Nannoperca australis). We integrate on‐the‐ground translocation efforts by volunteers from local communities, captive breeding by a private aquarium business, and genetic analyses done by a research institution to provide a holistic framework for the reintroduction of southern pygmy perch. We evaluated genetic diversity, population structure, relatedness, and inbreeding across the duration of the reintroduction program using data from neutral and adaptive genomic markers. This allowed us to assess the ability of such a program to minimize inbreeding and retain genomic variation, and to promote adaptive potential of the reintroduced population. While genetic variation for the source populations was very low, we found no decrease in genetic diversity or increase in inbreeding across the program. These genetic findings support the efforts made by local communities and will further inform future reintroductions as part of a collaborative conservation framework. We expand on our empirical case study by describing a theoretical framework for integrating conservation genomics research with community‐led conservation management programs and identifying the benefits of such a collaboration. Our study highlights the importance of multifaceted and integrated conservation management approaches to effectively protect and manage threatened species.
How populations of aquatic fauna persist in extreme desert environments is an enigma. Individuals often breed and disperse during favourable conditions. However, theory predicts that adaptive capacity should be low in small populations, such as in desert fishes. We integrated satellite-derived surface water data, neutral population dynamics and adaptive evolution to understand metapopulation persistence across the range of the desert rainbowfish, central Australia. Desert rainbowfish showed very small population sizes, especially at peripheral populations, and low connectivity between river catchments. Yet, there was no evidence of population-level inbreeding and there was adaptive divergence associated with aridity. Candidate adaptive genes included functions related to environmental cues and stressful conditions. Evolutionary modelling showed that selection in refugial sub-populations combined with connectivity during flood periods can enable retention of adaptive diversity. Our study demonstrates that adaptive evolution can occur in small populations and integrate with neutral metapopulation processes to allow persistence in the desert.