Conservation genomics and evolutionary potential of the southern pygmy perch, Nannoperca australis, in the Murray-Darling Basin, Australia

Author: Chris Brauer

Brauer, Chris, 2017 Conservation genomics and evolutionary potential of the southern pygmy perch, Nannoperca australis, in the Murray-Darling Basin, Australia, Flinders University, School of Biological Sciences

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Understanding how natural selection generates and maintains adaptive genetic diversity in heterogeneous environments is key to predicting the evolutionary responses of populations to rapid environmental change. The Murray-Darling Basin (MDB) is the largest source of water for agricultural irrigation in Australia and is one of the most fragile and threatened ecosystems in the country. Climate across the region is dominated by a steep gradient of aridity from east to west and hydroclimatic conditions are highly variable and unpredictable. Few areas remain unaffected by anthropogenic disturbance and current native fish populations represent just around 10% of pre-European settlement estimates. This work aims to investigate how environmental variation and human disturbance influence neutral and adaptive genetic variation, population connectivity and variation in gene expression of the southern pygmy perch (Nannoperca australis), a threatened freshwater fish undergoing rapid decline in the MDB. Here, I employed two next-generation sequencing methods, ddRAD and RNA-seq to assess adaptive resilience and evolutionary potential within an integrated riverscape genomics and comparative transcriptomics analytical framework. In the first riverscape genomics study of an Australian fish, high-resolution environmental data and 5,162 high-quality filtered SNPs were used to clarify spatial population structure and to assess footprints of selection associated with the hydroclimatic gradient and widespread human disturbance. Findings revealed strong neutral population structure consistent with spatial stream hierarchy, along with evidence that hydroclimatic variation and anthropogenic disturbance is driving local adaptive divergence of populations. These results contribute to understanding of adaptive evolution in highly fragmented ecosystems and suggest polygenic selection may largely underpin adaptive divergence in the wild. The consequences of habitat fragmentation for population persistence of freshwater biodiversity were then examined with a combination of riverscape genomics and individual-based population genetic simulations. Populations most isolated by recently constructed in-stream barriers showed reduced genetic diversity and increased genetic differentiation, even after accounting for the effects of natural stream hierarchy and environmental variation. These results provide first evidence that the decline of freshwater biodiversity across a riverine ecosystem can be directly attributed to anthropogenic habitat fragmentation. Finally, a de novo transcriptome was assembled and used to explore the roles of genetic and environmental variation in the evolution of plastic and divergent gene expression profiles among wild populations. Gene expression plasticity appeared unconstrained by genetic diversity, and comparative transcriptomic analyses identified divergently expressed candidate genes involved in metabolic responses to variations in water quality. These findings suggest that phenotypic plasticity can contribute to evolutionary potential of small populations, and highlight that the compounding effects of climate change and pollution likely pose additional extinction risks for many threatened species. Overall, the results in this thesis challenge the assumption that genetic drift will usually overwhelm selection in small, poorly dispersive populations. Instead, environmental variability within fragmented and disturbed habitat patches may maintain adaptive genetic variation, and drive the evolution of gene expression plasticity. The extent of recent demographic decline in response to severe habitat fragmentation however underscores the urgent need for well-considered proactive conservation measures to ensure persistence of the species in the MDB.

Keywords: Australia, climate change, conservation genetics, ddRAD-seq, RNA-seq, landscape genomics, comparative transcriptomics, Murray–Darling Basin, Nannoperca australis, pygmy perch, freshwater fish, habitat fragmentation

Subject: Biological Sciences thesis

Thesis type: Doctor of Philosophy
Completed: 2017
School: School of Biological Sciences
Supervisor: Prof Luciano Beheregaray