Phylogeographic history and evolutionary diversification of pygmy perches (Teleostei: Percichthyidae)

Author: Sean Buckley

Buckley, Sean, 2020 Phylogeographic history and evolutionary diversification of pygmy perches (Teleostei: Percichthyidae), Flinders University, College of Science and Engineering

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Analysing the environmental and evolutionary histories of species provides an empirical framework for testing biogeographic hypotheses and understanding factors underlying past, current and future demographic responses. Expanding these analyses to a comparative framework also allows for assessing the role of species-specific traits on biogeographic patterns, identifying whether species responses might be shared or not. The temperate zone of Australia is divided into two contrasting regions in the southeast and southwest corner of the mainland, with substantial spatial and temporal environmental variability in the southeast but with pronounced topographic and climatic stability since the Pliocene in the southwest. Several biological groups, such as pygmy perches, are common to both biogeographic regions, and present suitable systems to evaluate and compare the interaction of environmental and evolutionary histories. Additionally, all pygmy perch species are of conservation concern, and understanding the contribution of evolutionary history to their adaptive potential is important for guiding management strategies.

This work aims to investigate the phylogeographic histories of several pygmy perch lineages across the two temperate bioregions and to identify environmental factors underlying patterns of divergence and persistence. To achieve those aims, I first generated genome-wide (based on ddRAD) data to assess phylogenetic, demographic and population genetic patterns in pygmy perches from southeastern and southwestern Australia. These results were then integrated with environmental modelling for the two temperate regions to provide a more comprehensive assessment of their evolutionary histories. Complex coalescent modelling using 7,958 ddRAD loci containing 7,780 putatively unlinked SNPs revealed the spatial complexity of Plio-Pleistocene environmental changes on the evolutionary patterns of the southern pygmy perch (Nannoperca australis), a lineage from southeast Australia. The findings indicate that aridification played a stronger role in isolating inland populations compared to sea level changes in coastal populations. The Nannoperca australis patterns were compared with those inferred for the Yarra pygmy perch (Nannoperca obscura) across their co-distributed range. This analysis used 21,051 ddRAD loci and 17,389 SNPs for N. australis and 19,428 ddRAD loci and 15,715 SNPs for N. obscura. It revealed concordant demographic histories across a shared habitat refugium, but significant species-wide discordance in distribution patterns and connectivity. This disparity likely reflects differences in long-term standing genetic variation between species and may be a contributing factor to the variable success of recent conservation efforts for these threatened lineages.

Remarkably contrasting results were obtained for lineages endemic to the southwest Australia biodiversity hotspot in Western Australia. Here, populations belonging to the western pygmy perch species complex (Nannoperca vittata and Nannoperca pygmaea) were analysed using 19,426 ddRAD loci and 18,177 SNPs. The analyses revealed a number of anciently isolated lineages, including cryptic species, and reduced environmental fluctuations in this biodiversity hotspot, which allowed the accumulation and maintenance of pygmy perch diversity. A novel functional enrichment approach using fixed SNP differences was developed, which demonstrated potential mechanisms for reproductive isolation between cryptic species based on intracellular differences associated with chromosome arrangement.

Overall, these results illustrate the contrasting interplay between species evolutionary histories and environmental dynamics, with climatic stability allowing divergent lineages to persist but climatic variability creating more complex and fluctuating patterns of connectivity and persistence. Species responses to shared environmental change were not fully concordant and highlighted the role of intrinsic factors, such as genetic diversity, in allowing species to adapt to changing habitats. Altogether, environmental and species trait variation intersect to create an intricate network defining past species responses, adding to the complex nature of predicting adaptive resilience to environmental and climatic change. These findings provide important implications for the management of freshwater biota more widely, as well as specific to the pygmy perches, urging for protection of habitat for the newly identified lineages and informing ex situ and in situ conservation efforts.

Keywords: comparative phylogeography, species delimitation, genomics, fish, biogeography, coalescent, temperate Australia

Subject: Biology thesis

Thesis type: Doctor of Philosophy
Completed: 2020
School: College of Science and Engineering
Supervisor: Professor Luciano Beheregaray