Ecological disturbance influences adaptive divergence despite high gene flow in golden perch (Macquaria ambigua): Implications for management and resilience to climate change.

Populations that are adaptively divergent but maintain high gene flow may have greater resilience to environmental change as gene flow allows the spread of alleles that have already been tested elsewhere. In addition, populations naturally subjected to ecological disturbance may already hold resilience to future environmental change. Confirming this necessitates ecological genomic studies of high dispersal, generalist species. Here we perform one such study on golden perch (Macquaria ambigua) in the Murray-Darling Basin (MDB), Australia, using a genome-wide SNP data set. The MDB spans across arid to wet and temperate to subtropical environments, with low to high ecological disturbance in the form of low to high hydrological variability. We found high gene flow across the basin and three populations with low neutral differentiation. Genotype-environment association analyses detected adaptive divergence predominantly linked to an arid region with highly variable riverine flow, and candidate loci included functions related to fat storage, stress and molecular or tissue repair. The high connectivity of golden perch in the MDB will likely allow locally adaptive traits in its most arid and hydrologically variable environment to spread and be selected in localities that are predicted to become arid and hydrologically variable in future climates. High connectivity in golden perch is likely due to their generalist life history and efforts of fisheries management. Our study adds to growing evidence of adaptation in the face of gene flow and highlights the importance of considering ecological disturbance and adaptive divergence in biodiversity management.

Signatures of polygenic adaptation associated with climate across the range of a threatened fish species with high genetic connectivity.

Adaptive differences across species' ranges can have important implications for population persistence and conservation management decisions. Despite advances in genomic technologies, detecting adaptive variation in natural populations remains challenging. Key challenges in gene-environment association studies involve distinguishing the effects of drift from those of selection and identifying subtle signatures of polygenic adaptation. We used paired-end restriction site-associated DNA sequencing data (6,605 biallelic single nucleotide polymorphisms; SNPs) to examine population structure and test for signatures of adaptation across the geographic range of an iconic Australian endemic freshwater fish species, the Murray cod Maccullochella peelii. Two univariate gene-association methods identified 61 genomic regions associated with climate variation. We also tested for subtle signatures of polygenic adaptation using a multivariate method (redundancy analysis; RDA). The RDA analysis suggested that climate (temperature- and precipitation-related variables) and geography had similar magnitudes of effect in shaping the distribution of SNP genotypes across the sampled range of Murray cod. Although there was poor agreement among the candidate SNPs identified by the univariate methods, the top 5% of SNPs contributing to significant RDA axes included 67% of the SNPs identified by univariate methods. We discuss the potential implications of our findings for the management of Murray cod and other species generally, particularly in relation to informing conservation actions such as translocations to improve evolutionary resilience of natural populations. Our results highlight the value of using a combination of different approaches, including polygenic methods, when testing for signatures of adaptation in landscape genomic studies.

Genome-wide data delimits multiple climate-determined species ranges in a widespread Australian fish, the golden perch (Macquaria ambigua).

Species range limits often fluctuate in space and time in response to variation in environmental factors and to gradual niche evolution due to changes in adaptive traits. We used genome-wide data to investigate evolutionary divergence and species range limits in a generalist and highly dispersive fish species that shows an unusually wide distribution across arid and semi-arid regions of Australia. We generated ddRAD data (18,979 filtered SNPs and 1.725million bp of sequences) for samples from 27 localities spanning the native range of golden perch, Macquaria ambigua (Teleostei; Percichthyidae). Our analytical framework uses population genomics to assess connectivity and population structure using model-based and model-free approaches, phylogenetics to clarify evolutionary relationships, and a coalescent-based Bayesian species delimitation method to assess statistical support of inferred species boundaries. Addressing uncertainties regarding range limits and taxonomy is particularly relevant for this iconic Australian species because of the intensive stocking activities undertaken to support its recreational fishery and its predicted range shifts associated with ongoing climate change. Strong population genomic, phylogenetic, and coalescent species delimitation support was obtained for three separately evolving metapopulation lineages, each lineage should be considered a distinct cryptic species of golden perch. Their range limits match the climate-determined boundaries of main river basins, despite the ability of golden perch to cross drainage divides. We also identified cases suggestive of anthropogenic hybridization between lineages due to stocking of this recreationally important fish, as well as a potential hybrid zone with a temporally stable pattern of admixture. Our work informs on the consequences of aridification in the evolution of aquatic organisms, a topic poorly represented in the literature. It also shows that genome-scale data can substantially improve and rectify inferences about taxonomy, hybridization and conservation management previously proposed by detailed genetic studies.

The role of anthropogenic vs. natural in-stream structures in determining connectivity and genetic diversity in an endangered freshwater fish, Macquarie perch (Macquaria australasica).

Habitat fragmentation is one of the leading causes of population declines, threatening ecosystems worldwide. Freshwater taxa may be particularly sensitive to habitat loss as connectivity between suitable patches of habitat is restricted not only by the natural stream network but also by anthropogenic factors. Using a landscape genetics approach, we assessed the impact of habitat availability on population genetic diversity and connectivity of an endangered Australian freshwater fish Macquarie perch, Macquaria australasica (Percichthyidae). The relative contribution of anthropogenic versus natural in-stream habitat structures in shaping genetic structure and diversity in M. australasica was quite striking. Genetic diversity was significantly higher in locations with a higher river slope, a correlate of the species preferred habitat - riffles. On the other hand, barriers degrade preferred habitat and impede dispersal, contributing to the degree of genetic differentiation among populations. Our results highlight the importance of landscape genetics to understanding the environmental factors affecting freshwater fish populations and the potential practical application of this approach to conservation management of other freshwater organisms.

Islands of water in a sea of dry land: hydrological regime predicts genetic diversity and dispersal in a widespread fish from Australia's arid zone, the golden perch (Macquaria ambigua).

Rivers provide an excellent system to study interactions between patterns of biodiversity structure and ecological processes. In these environments, gene flow is restricted by the spatial hierarchy and temporal variation of connectivity within the drainage network. In the Australian arid zone, this variability is high and rivers often exist as isolated waterholes connected during unpredictable floods. These conditions cause boom/bust cycles in the population dynamics of taxa, but their influence on spatial genetic diversity is largely unknown. We used a landscape genetics approach to assess the effect of hydrological variability on gene flow, spatial population structure and genetic diversity in an Australian freshwater fish, Macquaria ambigua. Our analysis is based on microsatellite data of 590 samples from 26 locations across the species range. Despite temporal isolation of populations, the species showed surprisingly high rates of dispersal, with population genetic structure only evident among major drainage basins. Within drainages, hydrological variability was a strong predictor of genetic diversity, being positively correlated with spring-time flow volume. We propose that increases in flow volume during spring stimulate recruitment booms and dispersal, boosting population size and genetic diversity. Although it is uncertain how the hydrological regime in arid Australia may change under future climate scenarios, management strategies for arid-zone fishes should mitigate barriers to dispersal and alterations to the natural flow regime to maintain connectivity and the species' evolutionary potential. This study contributes to our understanding of the influence of spatial and temporal heterogeneity on population and landscape processes.

Comparative losses of quantitative and molecular genetic variation in finite populations of Drosophila melanogaster.

Quantitative genetic variation, the main determinant of the ability to evolve, is expected to be lost in small populations, but there are limited data on the effect, and controversy as to whether it is similar to that for near neutral molecular variation. Genetic variation for abdominal and sternopleural bristle numbers and allozyme heterozygosity were estimated in 23 populations of Drosophila melanogaster maintained at effective population sizes of 25, 50, 100, 250 or 500 for 50 generations, as well as in 19 highly inbred populations and the wild outbred base population. Highly significant negative regressions of proportion of initial genetic variation retained on inbreeding due to finite population size were observed for both quantitative characters (b = -0.67 +/- 0.14 and -0.58 +/- 0.11) and allozyme heterozygosity (b = -0.79 +/- 0.10), and the regression coefficients did not differ significantly. Thus, quantitative genetic variation is being lost at a similar rate to molecular genetic variation. However, genetic variation for all traits was lost at rates significantly slower than predicted by neutral theory, most likely due to associative overdominance. Positive, but relatively low correlations were found among the different measures of genetic variation, but their low magnitudes were attributed to large sampling errors, rather than differences in the underlying processes of loss.