Project

Ecological genomics of adaptation to environmental change

Goal: Rapid environmental and climatic change represents a clear and urgent challenge for conservation and evolutionary biologists – this is particularly so in aquatic ecosystems, which are experiencing some of the fastest rates of change. We are implementing a research program in ecological genomics to understand population adaptations and responses to environmental change in ecologically important aquatic organisms. Our program integrates comparative ecological genomics (in the wild and in the lab), phenotypic data and spatially-explicit modelling approaches to assess adaptation and vulnerability of aquatic biodiversity to environmental and climatic change.

For details about this and other similar research programs please visit:

http://www.molecularecology.flinders.edu.au/molecular-ecology-lab/research-programs/

Methods: RNA Sequencing, Genomics, Transcriptomics, Phenotyping, Genotype-Phenotype, Landscape Genetics, RAD-Seq, Ecological Genomics

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Luciano B Beheregaray
added a research item
Under climate change, 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 several narrow range endemic species 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.
Luciano B Beheregaray
added a research item
Significance Species with narrow distributions provide unique opportunities for understanding the mechanisms that limit their spread. We studied a marine invader that exhibits ecological dominance within its range and has the capacity to fundamentally alter the coastal habitat when introduced to new locations. We found evidence of the species’ potential to establish itself far beyond its present introduced range from both genomic data and species distribution modeling. Therefore, minor oceanographic changes (due to, for example, contemporary climate change) or alteration to human-mediated dispersal may trigger a large-scale invasion along vast stretches of coastlines. Our work provides a holistic framework to assess potential changes in the distribution of invasive species.
Luciano B Beheregaray
added a research item
The ecological impacts of increasing global temperatures are evident in most ecosystems on Earth, but our understanding of how climatic variation influences natural selection and adaptive resilience across latitudes is still largely unknown. Latitudinal gradients allow testing general ecosystem-level theories relevant to climatic adaptation. We assessed differences in adaptive diversity of populations along a latitudinal region spanning highly variable temperate to subtropical climates. We generated and integrated information from environmental mapping, phenotypic variation and genome-wide data from across the geographic range of the rainbowfish Melanotaenia duboulayi, an emerging aquatic system for studies of climate change. We detected, after controlling for spatial population structure, strong interactions between genotypes and environment associated to variation in stream flow and temperature. Some of these hydroclimate-associated genes were found to interact within functional protein networks that contain genes of adaptive significance for projected future climates in rainbowfish. Hydroclimatic selection was also associated with variation in phenotypic traits, including traits known to affect fitness of rainbowfish exposed to different flow environments. Consistent with predictions from the 'climatic variability hypothesis', populations exposed to extremes of important environmental variables showed stronger adaptive divergence and less variation in climate-associated genes compared to populations at the center of the environmental gradient. Our findings suggest that populations that evolved at environmental range margins and at geographic range edges may be more vulnerable to changing climates, a finding with implications for predicting adaptive resilience and managing biodiversity under climate change.
Luciano B Beheregaray
added a research item
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 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.
Luciano B Beheregaray
added 2 research items
We looked at the capacity of life to respond to future climates in three different regions: temperate and subtropical regions, and in deserts. We discovered a strong association between number of genes responding to projected temperatures and heat tolerance. The “winners” – those best at adapting to projected summer temperatures – evolved in the warm, subtropical regions. Those that evolved in cooler temperate ecosystems – the “losers” – risk becoming extinct. Desert species, which are predicted to be exposed to more extreme heatwaves and longer droughts in the future, are also vulnerable.
Significance Adaptation to climate change is expected to be influenced by thermal conditions experienced by species during their evolutionary history. We studied plastic capacity as a target of climatic selection, hypothesizing that populations that evolved under warmer climates have greater plastic adaptive resilience to climate change. This was tested experimentally by comparing upper thermal tolerance and gene expression in fish populations from desert, temperate, and subtropical regions of Australia. Divergent adaptive plastic responses to future climates were found across different bioregions, including in key heat stress genes. The greatest adaptive resilience was shown by the subtropical ecotype, followed by the desert and temperate ecotypes. These results have implications for large-scale assessments of climate impacts and for predictions of species distribution changes.
Luciano B Beheregaray
added a research item
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 world's best-defined marine thermal gradients (the South African coastline) to test the hypothesis that incipient ecological speciation is a result of 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 biogeographic regions based on 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 species, and biogeographic disjunctions in species assemblages. Our results indicate that temperature-mediated selection represents an early stage of marine ecological speciation in coastal regions that lack physical dispersal barriers.
Chris Brauer
added a research item
Dispersal and natural selection are key evolutionary processes shaping the distribution of phenotypic and genetic diversity. For species inhabiting complex spatial environments however, it is unclear how the balance between gene flow and selection may be influenced by landscape heterogeneity and environmental variation. Here we evaluated the effects of dendritic landscape structure and the selective forces of hydroclimatic variation on population genomic parameters for the Murray River rainbowfish, Melanotaenia fluviatilis across the Murray‐Darling Basin, Australia. We genotyped 249 rainbowfish at 17,503 high‐quality SNP loci and integrated these with models of network connectivity and high resolution environmental data within a riverscape genomics framework. We tested competing models of gene flow before using multivariate genotype‐environment association (GEA) analysis to test for signals of adaptive divergence associated with hydroclimatic variation. Patterns of neutral genetic variation were consistent with expectations based on the stream hierarchy model and M. fluviatilis’ moderate dispersal ability. Models incorporating dendritic network structure suggested that landscape heterogeneity is a more important factor determining connectivity and gene flow than waterway distance. Extending these results, we also introduce a novel approach to controlling for the unique effects of dendritic network structure in GEA analyses of populations of aquatic species. We identified 146 candidate loci potentially underlying a polygenic adaptive response to seasonal fluctuations in stream flow and variation in the relative timing of temperature and precipitation extremes. Our findings underscore an emerging predominant role for seasonal variation in hydroclimatic conditions driving local adaptation and are relevant for informing proactive conservation management. This article is protected by copyright. All rights reserved.
Luciano B Beheregaray
added 2 research items
Genetic datasets of tens of markers have been superseded through next-generation sequencing technology with genome-wide datasets of thousands of markers. Genomic datasets improve our power to detect low population structure and identify adaptive divergence. The increased population-level knowledge can inform the conservation management of endangered species, such as the blue whale (Balaenoptera musculus). In Australia, there are two known feeding aggregations of the pygmy blue whale (B. m. brevicauda) which have shown no evidence of genetic structure based on a small dataset of 10 microsatellites and mtDNA. Here, we develop and implement a high-resolution dataset of 8294 genome-wide filtered single nucleotide polymorphisms, the first of its kind for blue whales. We use these data to assess whether the Australian feeding aggregations constitute one population and to test for the first time whether there is adaptive divergence between the feeding aggregations. We found no evidence of neutral population structure and negligible evidence of adaptive divergence. We propose that individuals likely travel widely between feeding areas and to breeding areas, which would require them to be adapted to a wide range of environmental conditions. This has important implications for their conservation as this blue whale population is likely vulnerable to a range of anthropogenic threats both off Australia and elsewhere.
Spatial and temporal scales at which processes modulate genetic diversity over the landscape are usually overlooked, impacting the design of conservation management practices for widely distributed species. We examine processes shaping population divergence in highly mobile species by re-assessing the case of panmixia in the iconic olive ridley turtle from the eastern Pacific. We implemented a biophysical model of connectivity and a seascape genetic analysis based on nuclear DNA variation of 634 samples collected from 27 nesting areas. Two genetically distinct populations largely isolated during reproductive migrations and mating were detected, each composed of multiple nesting sites linked by high connectivity. This patternwas strongly associated with a steep environmental gradient and also influenced by ocean currents. These findings relate to meso-scale features of a dynamic oceanographic interface in the eastern tropical Pacific (ETP) region, a scenario that possibly provides different cost–benefit solutions and selective pressures for sea turtles during both the mating and migration periods.We reject panmixia and propose a new paradigm for olive ridley turtles where reproductive isolation due to assortative mating is linked to its environment. Our study demonstrates the relevance of integrative approaches for assessing the role of environmental gradients and oceanographic currents as drivers of genetic differentiation in widely distributed marine species. This is relevant for the conservation management of species of highly mobile behaviour, and assists the planning and development of large-scale conservation strategies for the threatened olive ridley turtles in the ETP. © 2018 The Author(s) Published by the Royal Society. All rights reserved.
Luciano B Beheregaray
added 2 research items
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 dataset. The MDB spans across arid to wet and temperate to sub-tropical 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. This article is protected by copyright. All rights reserved.
Chris Brauer
added a research item
Understanding whether small populations with low genetic diversity can respond to rapid environmental change via phenotypic plasticity is an outstanding research question in biology. RNA sequencing (RNA-seq) has recently provided the opportunity to examine variation in gene expression, a surrogate for phenotypic variation, in non-model species. We used a comparative RNA-seq approach to assess expression variation within and among adaptively divergent populations of a threatened freshwater fish, Nannoperca australis, found across a steep hydroclimatic gradient in the Murray-Darling Basin, Australia. These populations evolved under contrasting selective environments (e.g. dry/hot lowland; wet/cold upland) and represent opposite ends of the species’ spectrum of genetic diversity and population size. We tested the hypothesis that environmental variation among isolated populations has driven the evolution of divergent expression at ecologically important genes using differential expression (DE) analysis and an ANOVA-based comparative phylogenetic expression variance and evolution model framework based on 27,425 de novo assembled transcripts. Additionally, we tested whether gene expression variance within-populations was correlated with levels of standing genetic diversity. We identified 290 DE candidate transcripts, 33 transcripts with evidence for high expression plasticity, and 50 candidates for divergent selection on gene expression after accounting for phylogenetic structure. Variance in gene expression appeared unrelated to levels of genetic diversity. Functional annotation of the candidate transcripts revealed variation in water quality is an important factor influencing expression variation for N. australis. Our findings suggest that gene expression variation can contribute to the evolutionary potential of small populations. This article is protected by copyright. All rights reserved.
Luciano B Beheregaray
added a research item
Transcriptomics via RNA-seq has rapidly emerged as a powerful tool for ecological and evolutionary studies, enabling genome-scale studies of adaptation via regulation of global gene expression. Here we present a de novo transcriptome for the desert rainbowfish (Melanotaenia splendida tatei) based on individuals sampled in the Lake Eyre Basin, Australia's arid zone river system. Recently developed methods in RNA-seq and bioinformatics were used for sequencing, assembling and annotating a high-quality liver transcriptome suitable for studies of ecology and adaptation in desert rainbowfish. Transcript annotation in UniprotKB using BLASTx assigned unique protein matches to ~ 47% of 116,092 Trinity genes, while BLASTp assigned unique protein matches to ~ 35% of 62,792 predicted protein-coding regions. A full Trinotate annotation report is provided for predicted genes and their corresponding transcripts. Annotations were compared with previously identified genes for transcriptional regulation and heritable plasticity in future climates in the subtropical rainbowfish (M. duboulayi), finding ~ 57% of these candidate genes present in the desert rainbowfish transcriptome. We discuss the utility of transcriptomics methods for ecological studies of adaptation, while emphasising a range of methodological considerations for dealing with transcriptome datasets. This newly assembled transcriptome is expected to help elucidate mechanisms for adaptation to high temperatures and a variable climate in desert aquatic fauna.
Luciano B Beheregaray
added 2 research items
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 and 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 1.725 million 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.
Luciano B Beheregaray
added a research item
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 1.725 million 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.
Peter Teske
added a research item
Distinguishing the relative influence of historic (i.e. natural) versus anthropogenic factors in metapopulation structure is an important but often overlooked step in management programs of threatened species. Biotas in freshwater wetlands and floodplains, such as those in the Murray–Darling Basin (MDB)—one of Australia’s most impacted ecosystems, are particularly susceptible to anthropogenic fragmentation. Here we present a comprehensive multilocus assessment of genetic variation in the threatened southern pygmy perch Nannoperca australis (578 individuals; 45 localities; microsatellite, allozyme and mitochondrial DNA datasets), an ecological specialist with low dispersal potential. We assess patterns of spatial structure and genetic diversity in populations spanning the highly fragmented MDB and test whether recent anthropogenic modification has disrupted range-wide connectivity. We detected strong and hierarchical population structure, very low genetic diversity and lack of contemporary gene flow across the MDB. In contrast, the apparent absence of pronounced or long-term phylogeographic structure suggests that observed population divergences generally do not reflect deeply historic natural fragmentation. Coalescent-based analyses supported this inference, revealing that divergence times between populations from the upper and lower MDB fall into the period of European settlement. It appears that the observed contemporary isolation of populations is partly explained by the severe modification of the MDB post-dating the onset of European settlement. Our integrated approach substantially improves the interpretation of how fragmentation impacts present-day biodiversity. It also provides novel contributions for risk-assessing management actions in the context of captive breeding and translocations of small freshwater fishes, a group of increasing global conservation concern.
Luciano B Beheregaray
added 2 research items
Captive breeding programs are often a necessity for the continued persistence of a population or species. They typically have the goal of maintaining genetic diversity and minimizing inbreeding. However, most captive breeding programs have been based on the assumption that the founding breeders are unrelated and outbred, even though in situ anthropogenic impacts often mean these founders may have high relatedness and substantial inbreeding. In addition, polygamous group-breeding species in captivity often have uncertain pedigrees, making it difficult to select the group composition for subsequent breeding. Molecular-based estimates of relatedness and inbreeding may instead be use to select breeding groups (≥ two individuals) that minimize relatedness and filter out inbred individuals. SWINGER constructs breeding groups based on molecular estimates of relatedness and inbreeding. The number of possible combinations of breeding groups quickly becomes intractable by hand. SWINGER was designed to overcome this major issue in ex situ conservation biology. The user can specify parameters within SWINGER to reach breeding solutions that suit the mating system of the target species and available resources. We provide evidence of the efficiency of the software with an empirical example and using simulations. The only data required is a typical molecular marker dataset, such as a microsatellite or SNP dataset, from which estimates of inbreeding and pairwise relatedness may be obtained. Such molecular datasets are becoming easier to gather from non-model organisms with next-generation sequencing (NGS) technology. SWINGER is an open source software with a user-friendly interface and is available at http:// www.molecularecology . flinders.edu.au/molecular-ecology-lab/software/swinger/swinger/ and https://github.com/Yuma248/Swinger This article is protected by copyright. All rights reserved.
Luciano B Beheregaray
added a research item
Poor dispersal species represent conservative benchmarks for biodiversity management because they provide insights into ecological processes influenced by habitat fragmentation that are less evident in more dispersive organisms. Here we used the poorly dispersive and threatened river blackfish (Gadopsis marmoratus) as a surrogate indicator system for assessing the effects of fragmentation in highly modified river basins and for prioritizing basin-wide management strategies. We combined individual, population and landscape-based approaches to analyze genetic variation in samples spanning the distribution of the species in Australia’s Murray–Darling Basin, one of the world’s most degraded freshwater systems. Our results indicate that G. marmoratus displays the hallmark of severe habitat fragmentation with notably scattered, small and demographically isolated populations with very low genetic diversity—a pattern found not only between regions and catchments but also between streams within catchments. By using hierarchically nested population sampling and assessing relationships between genetic uniqueness and genetic diversity across populations, we developed a spatial management framework that includes the selection of populations in need of genetic rescue. Landscape genetics provided an environmental criterion to identify associations between landscape features and ecological processes. Our results further our understanding of the impact that habitat quality and quantity has on habitat specialists with similarly low dispersal. They should also have practical applications for prioritizing both large- and small-scale conservation management actions for organisms inhabiting highly fragmented ecosystems.
Luciano B Beheregaray
added 2 research items
Evolution creates and sustains biodiversity via adaptive changes in ecologically relevant traits. Ecologically mediated selection contributes to genetic divergence both in the presence or absence of geographic isolation between populations, and is considered an important driver of speciation. Indeed, the genetics of ecological speciation is becoming increasingly studied across a variety of taxa and environments. In this paper we review the literature of ecological speciation in the tropics. We report on low research productivity in tropical ecosystems and discuss reasons accounting for the rarity of studies. We argue for research programs that simultaneously address biogeographical and taxonomic questions in the tropics, while effectively assessing relationships between reproductive isolation and ecological divergence. To contribute toward this goal, we propose a new framework for ecological speciation that integrates information from phylogenetics, phylogeography, population genomics, and simulations in evolutionary landscape genetics (ELG). We introduce components of the framework, describe ELG simulations (a largely unexplored approach in ecological speciation), and discuss design and experimental feasibility within the context of tropical research. We then use published genetic datasets from populations of five codistributed Amazonian fish species to assess the performance of the framework in studies of tropical speciation. We suggest that these approaches can assist in distinguishing the relative contribution of natural selection from biogeographic history in the origin of biodiversity, even in complex ecosystems such as Amazonia. We also discuss on how to assess ecological speciation using ELG simulations that include selection. These inte-grative frameworks have considerable potential to enhance conservation management in biodiversity rich ecosystems and to complement historical biogeographic and evolutionary studies of tropical biotas.
Chris Brauer
added an update
Very excited to start work on the project this week, beginning with a landscape genomic study of the Murray River rainbowfish (Melanotaenia fluviatilis).
 
Luciano B Beheregaray
added a project goal
Rapid environmental and climatic change represents a clear and urgent challenge for conservation and evolutionary biologists – this is particularly so in aquatic ecosystems, which are experiencing some of the fastest rates of change. We are implementing a research program in ecological genomics to understand population adaptations and responses to environmental change in ecologically important aquatic organisms. Our program integrates comparative ecological genomics (in the wild and in the lab), phenotypic data and spatially-explicit modelling approaches to assess adaptation and vulnerability of aquatic biodiversity to environmental and climatic change.
For details about this and other similar research programs please visit: