Population Genetic Diversity in the Australian ‘Seascape’: A Bioregion Approach

RESEARCH ARTICLE Population Genetic Diversity in the Australian ‘Seascape’: A Bioregion Approach Lisa C. Pope1*, Cynthia Riginos1, Jennifer Ovenden2, Jude Keyse1, Simon P. Blomberg1 1 School of Biological Sciences, The University of Queensland, Brisbane, Australia, 2 Molecular Fisheries Laboratory, School of Biomedical Sciences, The University of Queensland, Brisbane, Australia * Abstract OPEN ACCESS Citation: Pope LC, Riginos C, Ovenden J, Keyse J, Blomberg SP (2015) Population Genetic Diversity in the Australian ‘Seascape’: A Bioregion Approach. PLoS ONE 10(9): e0136275. doi:10.1371/journal. pone.0136275 Editor: Christopher J Fulton, The Australian National University, AUSTRALIA Received: October 26, 2014 Accepted: August 2, 2015 Published: September 16, 2015 Copyright: © 2015 Pope et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Genetic diversity within species may promote resilience to environmental change, yet little is known about how such variation is distributed at broad geographic scales. Here we develop a novel Bayesian methodology to analyse multi-species genetic diversity data in order to identify regions of high or low genetic diversity. We apply this method to co-distributed taxa from Australian marine waters. We extracted published summary statistics of population genetic diversity from 118 studies of 101 species and > 1000 populations from the Australian marine economic zone. We analysed these data using two approaches: a linear mixed model for standardised data, and a mixed beta-regression for unstandardised data, within a Bayesian framework. Our beta-regression approach performed better than models using standardised data, based on posterior predictive tests. The best model included region (Integrated Marine and Coastal Regionalisation of Australia (IMCRA) bioregions), latitude and latitude squared. Removing region as an explanatory variable greatly reduced model performance (delta DIC 23.4). Several bioregions were identified as possessing notably high genetic diversity. Genetic diversity increased towards the equator with a ‘hump’ in diversity across the range studied (−9.4 to −43.7°S). Our results suggest that factors correlated with both region and latitude play a role in shaping intra-specific genetic diversity, and that bioregion can be a useful management unit for intra-specific as well as species biodiversity. Our novel statistical model should prove useful for future analyses of within species genetic diversity at broad taxonomic and geographic scales. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: LP was funded to perform this work by The University of Queensland, UQ Postdoctoral Research Fellowships for Women, part-time (http://www.uq.edu. au/research/research-management/uq-postdoctoralresearch-fellowships-for-women). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Introduction Genetic diversity can be considered the most basic level of biodiversity [1,2]. The need to conserve genetic diversity is being increasingly recognised by management agencies globally (e.g. [3]), with growing evidence that populations with higher levels of genetic diversity have greater resilience to changing and unpredictable environments [4,5]. Unlike global patterns of species diversity, which show strong latitudinal clines across a broad range of taxa, (e.g. [6,7]), it is yet to be established whether such patterns are common, or consistent, for within species genetic diversity across taxa (but see [8–14]). PLOS ONE | DOI:10.1371/journal.pone.0136275 September 16, 2015 1 / 19 Genetic Diversity in the Australian 'Seascape' Many factors will influence genetic diversity within populations. Neutral population genetic diversity is expected to be proportional to long-term effective population size and mutation [15], which is influenced by a wide range of factors such as: dispersal [16], breeding system [17], historic population size [18], and present-day abundance (e.g. [19] (nuclear only); [20]). It has been suggested that some of the same factors hypothesised to influence species richness could also influence genetic diversity. Such factors are often correlated with latitude, and include: increased mutation rates or relaxed metabolism constraints caused by higher temperatures (e.g. [21,22]); more stable, older populations [23]; and higher density due to greater food availability/niche diversity (e.g. [24]). As for many other species, marine species richness is strongly correlated with latitude, declining away from the equator in coastal species [7,25]. If there is a correlation between species richness and population genetic diversity, termed the species genetic diversity correlation (SGDC; [12,26]), we expect a decline in genetic diversity away from the equator. Conversely, recent work has demonstrated that marine community evenness (number of individuals of each species) decreased towards the equator due to the presence of a greater number of rare species [27]. We might therefore predict a weaker relationship, or even a reduction in average intra-specific genetic diversity towards the equator due to greater variance in population size. Alternatively, differences among species in dispersal characteristics (e.g. [28]), life history strategy [29], or differences among populations due to factors such as range position (central vs edge populations, e.g. [30]), may not have strong geographic patterns, making concordant geographic patterns in population genetic diversity uncommon (e.g. [11]). Bioregions represent an attempt to delineate areas containing distinct species assemblages, common across a broad range of taxa. Such regions are likely to possess similarities in both evolutionary history and environmental characteristics, making them a useful unit for testing biogeographic hypotheses [31]. Common evolutionary processes may result in broad-scale patterns of genetic diversity [32], and regions may therefore be more informative than latitude for describing intra-specific diversity. Extensive effort has been placed into designating bioregions within the Australian marine environment, based on the distributions of fish and other species, and bathymetric and environmental variables [33]. This regional framework, the Integrated Marine and Coastal Regionalisation of Australia (IMCRA), has been used to determine representative regions for conservation and management around Australia. However, the relevance of these regions to the distribution of intra-specific genetic diversity is unknown. In order to determine within species genetic diversity pat (...truncated)