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Beheregaray, L. B.

Publications and source records attributed to Beheregaray, L. B..

17 recordsLinked to original sources

From tropical rainforests to scorching deserts: biogeography shapes climate-change plasticity in Australian rainbowfishes

Thermal tolerance and the plasticity of regulatory mechanisms are likely to influence biodiversity persistence under global warming. Continental-scale assessments of physiological resilience and gene expression plasticity within a closely related clade are rare, yet they could reveal how bioregional climatic history shapes vulnerability to climate warming. We used a comparative approach across five climatic ecotypes of Australian rainbowfishes (tropical rainforest, tropical savannah, subtropical, desert, and temperate) to investigate variation in thermal tolerance and gene expression plasticity in response to warming. We reconstructed phylogenetic relationships among these ecotypes, estimated their ecological niches and environmental warming tolerance, and experimentally measured CTMAX and global gene expression responses to a projected summer heat event. Closely related ecotypes showed divergent bioclimatic niches, contrasting sensitivities to warming, and extensive but idiosyncratic expression responses to heat stress. Plastic responses to warming, including in key heat stress genes, were positively associated with thermal tolerance across ecotypes. The tropical savannah and subtropical ecotypes, both from environmentally variable bioregions, showed extensive transcriptional responses to warming and high thermal tolerance. The desert ecotype was intermediate for both traits, whereas the temperate ecotype showed the most limited transcriptional response and lowest thermal tolerance. In contrast, the tropical rainforest ecotype showed limited plasticity, potentially reflecting local adaptation to milder, more stable conditions and more specialised thermal responses. Our findings support the hypothesis that bioregional climatic history shapes broad patterns of climate resilience, including thermal tolerance and transcriptional plasticity, and may influence which combinations of traits are favoured under future climates.

ecology↗

Tropical rainforest versus savannah: Biome-specific landscape structure mediates adaptive strategies and resilience to environmental change

As ecosystems face rapid environmental change, understanding the interplay between landscape structure, genetic diversity, and adaptive potential is critical for predicting resilience. We investigated how biome-specific connectivity and environmental heterogeneity mediate adaptive strategies and resilience in the tropical rainbowfish (Melanotaenia splendida splendida) across contrasting rainforest and savannah ecosystems in tropical Australia. Using an integrative framework combining genomic, morphological, and environmental analyses, we inferred that hydroclimatic variation has been a key driver of genetic and phenotypic divergence. Rainforest populations exhibited strong local adaptation to fragmented, stable environments, while savannah populations showed less genomic differentiation and morphological divergence, patterns consistent with weaker local adaptation. We hypothesise that greater reliance on phenotypic plasticity may facilitate adaptive responses in savannah populations, reflecting their exposure to more connected and variable environments. Variance partitioning highlighted the contrasting roles of neutral and adaptive processes across biomes, with implications for managing resilience in freshwater systems under climate change. Our findings underscore the trade-offs between connectivity, local adaptation, and plasticity, providing a model for understanding adaptation and resilience across diverse ecosystems.

ecology↗

Environmental gradients decouple demographic and adaptive connectivity in a highly mobile coastal marine species

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 14,699 SNPs, we identified two distinct 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 throughout both eastern and western regions, while candidate adaptive loci revealed substantially reduced connectivity, especially for Northern Spencer Gulf and West Coast populations. This pattern of locally restricted gene flow at adaptive genomic regions suggests that strong environmental gradients are driving adaptive divergence 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.

ecology↗

Estimation of effective population size and effective number of breeders in an abundant and heavily exploited marine teleost

Obtaining reliable estimates of the effective number of breeders N(b) 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 upwards modifications of our estimates, demonstrating the importance of applying these bias corrections. Our findings provide important guidelines for estimatingNb 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.

genomics↗

Connecting the dots: applying multispecies connectivity in marine park networkplanning

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 used intraspecific genetic and genomic data for five marine species with varying life histories 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 other protected networks with intraspecies genetic data.

ecology↗

Long-term climatic stability drives accumulation and maintenance of divergent lineages in a temperate biodiversity hotspot

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 in 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.

evolutionary biology↗

Bioregional boundaries and genomically-delineated stocks in snapper (Chrysophrys auratus) from southeastern Australia

Marine species often exhibit genetic discontinuities concordant with biogeographic boundaries, frequently occurring due to changes in ocean circulation, bathymetry, coastline topography and temperature. Here we used 10,916 single nucleotide polymorphisms (SNPs) to assess the concordance between population genomic differentiation and coastal biogeography in the fishery important snapper (Chrysophrys auratus) across southeastern Australia. Additionally, we investigated whether spatial scales of assessment and management of snapper align with evidence from population genomics. Across 488 snapper samples from 11 localities between the west coast of South Australia and the south coast of New South Wales, we detected genomic structure concordant with the regions three biogeographic provinces. We also detected fine-scale genetic structuring relating to spatial variation in spawning and recruitment dynamics, as well as temporal stability in the genomic signal associated with two important spawning grounds. The current management boundaries in the region coincided with either the genetic breaks at bioregional boundaries or with localscale variation. Our study highlights the value of population genomic surveys in species with high dispersal potential for uncovering stock boundaries and demographic variation related to spawning and recruitment. It also illustrates the importance of marine biogeography in shaping population structure in commercial species with high dispersal potential.

genomics↗

Natural hybridisation reduces vulnerability to climate change

Understanding how species can respond to climate change is a major global challenge. Species unable to track their niche via range shifts are largely reliant on genetic variation to adapt and persist. Genomic vulnerability predictions are used to identify populations that lack the necessary variation, particularly at climate relevant genes. However, hybridization as a source of novel adaptive variation is typically ignored in genomic vulnerability studies. We estimated environmental niche models and genomic vulnerability for closely related species of rainbowfish (Melanotaenia spp.) across an elevational gradient in the Australian wet tropics. Hybrid populations between a widespread generalist and narrow range endemics exhibited reduced vulnerability to projected climates compared to pure narrow endemics. Overlaps between introgressed and adaptive genomic regions were consistent with a signal of adaptive introgression. Our findings highlight the often-underappreciated conservation value of hybrid populations and indicate that adaptive introgression may contribute to evolutionary rescue of species with narrow environmental ranges.

evolutionary biology↗

Environmental selection, rather than neutral processes, best explain patterns of diversity in a tropical rainforest fish

To conserve the high functional and genetic variation in hotspots such as tropical rainforests, it is essential to understand the forces driving and maintaining biodiversity. We asked to what extent environmental gradients and terrain structure affect morphological and genomic variation across the wet tropical distribution of an Australian rainbowfish, Melanotaenia splendida splendida. We used an integrative riverscape genomics and morphometrics framework to assess the influence of these factors on both putative adaptive and non-adaptive spatial divergence. We found that neutral genetic population structure was largely explainable by restricted gene flow among drainages. However, environmental associations revealed that ecological variables had a similar power to explain overall genetic variation, and greater power to explain body shape variation, than the included neutral covariables. Hydrological and thermal variables were the best environmental predictors and were correlated with traits previously linked to heritable habitat-associated dimorphism in rainbowfishes. Additionally, climate-associated genetic variation was significantly associated with morphology, supporting heritability of shape variation. These results support the inference of evolved functional differences among localities, and the importance of hydroclimate in early stages of diversification. We expect that substantial evolutionary responses will be required in tropical rainforest endemics to mitigate local fitness losses due to changing climates.

evolutionary biology↗

Fisheries genomics of snapper (Chrysophrys auratus) along the western Australian coast

The efficacy of fisheries management strategies depends on stock assessment and management actions being carried out at appropriate spatial scales. This requires understanding of spatial and temporal population structure and connectivity, which is challenging in weakly structured and highly connected marine populations. We carried out a population genomics study of the heavily exploited snapper (Chrysophrys auratus) along [~]2,600 km of the Australian coastline, with a focus on Western Australia (WA). We used 10,903 filtered SNPs in 341 individuals from eight locations to characterise population structure and connectivity in snapper across WA and to assess if current spatial scales of stock assessment and management agree with evidence from population genomics. Our dataset also enabled us to investigate temporal stability in population structure as well as connectivity between WA and its nearest, eastern jurisdictional neighbor. As expected for a species influenced by the extensive ocean boundary current in the region, low genetic differentiation and high connectivity was uncovered across WA. However, we did detect strong isolation by distance and genetic discontinuities in the mid-west and south-east. The discontinuities correlate with boundaries between biogeographic regions, influenced by on-shelf oceanography, and the sites of important spawning aggregations. We also detected temporal instability in genetic structure at one of our sites, possibly due to interannual variability in recruitment in adjacent regions. Our results partly contrast with the current spatial management of snapper in WA, highlighting the need for a review. This study supports the value of population genomic surveys in informing the management of weakly-structured and wide-ranging marine fishery resources.

genomics↗

Variation in intraspecific demography drives localised concordance but species-wide discordance in responses to Plio-Pleistocene climatic change

Understanding how species biology may facilitate resilience to climate change remains a critical factor in detecting and protecting species at risk of extinction. Many studies have focused on the role of particular ecological traits in driving species responses, but less so on demographic history and levels of standing genetic variation. We used environmental and genomic datasets to reconstruct the phylogeographic histories of two ecologically similar and largely co-distributed freshwater fishes to assess the degree of concordance in their responses to Plio-Pleistocene climatic changes. Although several co-occurring populations demonstrated concordant demographic histories, idiosyncratic population size changes were found at the range edges of the more spatially restricted species. Discordant responses between species were associated with low standing genetic variation in peripheral populations. This might have hindered adaptive potential, as documented in recent population declines and extinctions of the two species. Our results highlight both the role of spatial scale in the degree of concordance in species responses to climate change, and the importance of standing genetic variation in facilitating range shifts. Even when ecological traits are similar between species, long-term genetic diversity and historical population demography may lead to discordant responses to ongoing and future climate change.

evolutionary biology↗

Recent and rapid anthropogenic habitat fragmentation increases extinction risk for freshwater biodiversity

Anthropogenic habitat fragmentation is often implicated as driving the current global extinction crisis, particularly in freshwater ecosystems. The genetic signal of recent population isolation can however be confounded by the complex spatial arrangement of dendritic river systems. Consequently, many populations may presently be managed separately based on an incorrect assumption that they have evolved in isolation. Integrating landscape genomics data with models of connectivity that account for landscape structure, we show that the cumulative effects of multiple in-stream barriers have contributed to the recent decline of a freshwater fish from the Murray-Darling Basin, Australia. In addition, individual-based eco-evolutionary simulations further demonstrate that contemporary inferences about population isolation are consistent with the 160-year time frame since construction of in-stream barriers began in the region. Our findings suggest that the impact of very recent fragmentation may be often underestimated for freshwater biodiversity. We argue that proactive conservation measures to reconnect many riverine populations are urgently needed.

ecology↗

The roles of aridification and sea level changes in the diversification and persistence of freshwater fish lineages

While the influence of Pleistocene climatic changes on divergence and speciation has been well-documented across the globe, complex spatial interactions between hydrology and eustatics over longer timeframes may also determine species evolutionary trajectories. Within the Australian continent, glacial cycles were not associated with changes in ice cover and instead largely resulted in fluctuations from moist to arid conditions across the landscape. Here, we investigate the role of hydrological and coastal topographic changes brought about by Plio-Pleistocene climatic changes on the biogeographic history of a small Australian freshwater fish, the southern pygmy perch Nannoperca australis. Using 7,958 ddRAD-seq (double digest restriction-site associated DNA) loci and 45,104 filtered SNPs, we combined phylogenetic, coalescent and species distribution analyses to investigate the relative roles of aridification, sea level and tectonics and their associated biogeographic changes across southeast Australia. Sea-level changes since the Pliocene and reduction or disappearance of large waterbodies throughout the Pleistocene were determining factors in strong divergence across the clade, including the initial formation and maintenance of a cryptic species, N. flindersi. Isolated climatic refugia and fragmentation due to lack of connected waterways maintained the identity and divergence of inter- and intraspecific lineages. Our historical findings suggest that predicted increases in aridification and sea level due to anthropogenic climate change might result in markedly different demographic impacts, both spatially and across different landscape types.

evolutionary biology↗

Adaptation of plasticity to predicted climates in Australian rainbowfishes (Melanotaenia) across climatically defined bioregions

Resilience to environmental stressors due to climate warming is influenced by local adaptations, including the capacity for plastic responses. The recent literature has focussed on genomic signatures of climatic adaptation, however little work has been done to address how plastic capacity may be influenced by biogeographic history and evolutionary processes. Here, we investigate phenotypic plasticity as a target of climatic selection, hypothesising that lineages that evolved under warmer climate will exhibit greater plastic adaptive resilience to thermal stress. This was tested using common garden experiments to compare gene expression regulation within and among a temperate, a subtropical and a desert ecotype of Australian rainbowfish. Individuals from each ecotype were subjected to contemporary and projected summer thermal conditions for 2070, and their global patterns of gene expression were characterized using liver transcriptomes. Critical thermal maximums were also determined for each ecotype to assess thermal tolerance. A comparative phylogenetic expression variance and evolution model framework was used to assess plastic and evolved changes in gene expression. Similar changes in both the direction and the magnitude of expressed genes were found within ecotypes. Although most expressed genes were identified in all ecotypes, 532 genes were identified as candidates subject to ecotype-specific directional selection. Twenty-three of those genes showed signal of adaptive (i.e. genetic-based) plastic response to future increases in temperature. Network analyses demonstrated centrality of these genes in thermal response pathways, along with several highly conserved hub genes thought to be integral for heat stress responses. The greatest adaptive resilience to warming was shown by the subtropical ecotype, followed by the desert and temperate ecotypes. Our findings indicate that vulnerability to climate change will be highly influenced by biogeographic factors, and we stress the need for integrative assessments of climatic adaptive traits for accurate estimations of population and ecosystem responses.

ecology↗

Thermal selection drives biodiversity origination across the Atlantic/Indian Ocean boundary

Intraspecific genetic structure in widely distributed marine species often mirrors the boundaries between temperature-defined bioregions. This suggests that the same thermal gradients that maintain distinct species assemblages also drive the evolution of new biodiversity. Ecological speciation scenarios are often invoked to explain such patterns, but the fact that adaptation is usually only identified when phylogenetic splits are already evident makes it impossible to rule out the alternative scenario of allopatric speciation with subsequent adaptation. We integrated large-scale genomic and environmental datasets along one of the worlds best defined marine thermal gradients (the South African coastline) to test the hypothesis that incipient speciation in the sea is due to divergence linked to the thermal environment. We identified temperature-associated gene regions in a coastal fish species that is spatially homogeneous throughout several temperature-defined biogeographical regions on the basis of selectively neutral markers. Based on these gene regions, the species is divided into geographically distinct regional populations. Importantly, the ranges of these populations are delimited by the same ecological boundaries that define distinct infraspecific genetic lineages in co-distributed marine the species, and biogeographical disjunctions in species assemblages. Our results indicate that ecologically-mediated selection represents an early stage of marine speciation in coastal regions that lack physical dispersal barriers.

evolutionary biology↗

Theory, practice, and conservation in the age of genomics: the Galapagos giant tortoise as a case study

High-throughput DNA sequencing allows efficient discovery of thousands of single nucleotide polymorphisms (SNPs) in non-model species. Population genetic theory predicts that this large number of independent markers should provide detailed insights into population structure, even when only a few individuals are sampled. Still, sampling design can have a strong impact on such inferences. Here, we use simulations and empirical SNP data to investigate the impacts of sampling design on estimating genetic differentiation among populations that represent three species of Galapagos giant tortoises (Chelonoidis spp.). Though microsatellite and mitochondrial DNA analyses have supported the distinctiveness of these species, a recent study called into question how well these markers matched with data from genomic SNPs, thereby questioning decades of studies in non-model organisms. Using >20,000 genome-wide SNPs from 30 individuals from three Galapagos giant tortoise species, we find distinct structure that matches the relationships described by the traditional genetic markers. Furthermore, we confirm that accurate estimates of genetic differentiation in highly structured natural populations can be obtained using thousands of SNPs and 2-5 individuals, or hundreds of SNPs and 10 individuals, but only if the units of analysis are delineated in a way that is consistent with evolutionary history. We show that the lack of structure in the recent SNP-based study was likely due to unnatural grouping of individuals and erroneous genotype filtering. Our study demonstrates that genomic data enable patterns of genetic differentiation among populations to be elucidated even with few samples per population, and underscores the importance of sampling design. These results have specific implications for studies of population structure in endangered species and subsequent management decisions.\n\n\"Modern molecular techniques provide unprecedented power to understand genetic variation in natural populations. Nevertheless, application of this information requires sound understanding of population genetics theory.\"\n\n- Fred Allendorf (2017, p. 420)

evolutionary biology↗

Reviving A Lost Species: The Case Of The Floreana Galapagos Giant Tortoise Chelonoidis elephantopus

Species are being lost at an unprecedented rate due to human-driven environmental changes. The cases in which species declared extinct can be revived are rare. However, here we report that a remote volcano in the Galapagos Islands hosts many giant tortoises with high ancestry from a species previously declared as extinct: Chelonoidis elephantopus or the Floreana tortoise. Of 150 individuals with distinctive morphology sampled from the volcano, genetic analyses revealed that 65 had C. elephantopus ancestry and thirty-two were translocated from the volcanos slopes to a captive breeding center. A genetically informed captive breeding program now being initiated will, over the next decades, return C. elephantopus tortoises to Floreana Island to serve as engineers of the islands ecosystems. Ironically, it was the haphazard translocations by mariners killing tortoises for food centuries ago that created the unique opportunity to revive this \"lost\" species today.

evolutionary biology↗