Connecting the past, present and future: A population genomic study of Australasian snapper (Chrysophrys auratus) in New Zealand

Advances in genomic methods now enable the study of wild populations and their evolutionary history at an unprecedented level. The genotyping of many thousands of genetic markers across the genome provides high statistical resolution. This enables the identification of adaptive genetic variation, providing novel insights into population demography and the processes driving population divergence. Marine fish are ideal candidates to study the processes driving evolutionary divergence because selection works efficiently in large populations, and marine populations can be distributed over large spatial ranges and occupy a range of environmental conditions. This thesis used whole-genome variant data to study the Australasian snapper (Chrysophrys auratus, tāmure) in New Zealand. Snapper is one of New Zealand’s largest inshore fisheries and has experienced significant population reductions. The aims of this thesis were to investigate the genome-wide variation in snapper in New Zealand and 1) assess the neutral and adaptive population genetic structure, 2) reconstruct the demographic history, and 3) identify genomic regions, genes and their functions that show signs of selection. Population genomic structure was assessed using whole-genome resequencing data from 350 individuals, and this data set resulted in 167,543 assumed neutrally evolving loci (SNPs). It was found that levels of genetic diversity were not significantly different between populations, suggesting that fishing pressure has not lead to local reductions in genetic variation. Levels of genetic differentiation between sampled populations was low, with significant evidence for isolation by distance (R2 = 0.75, p = 0.002). Pairwise FST estimates and PCA/DAPC showed the presence of two genetic clusters, one containing the northern and one containing the southern populations. Genetic disjunctions combined with mixing between the clusters was detected around the Mahia peninsula and Cape Reinga. The identification of adaptive loci enabled the identification of fine-scale population structure, reflecting currently recognized stocks. The ability to differentiate between stocks is fundamental for fisheries management. The patterns detected here show promising results for future implementation into fisheries management of snapper stocks. Contemporary and ancient mitochondrial genomes were used to assess the demographic, and phylogeographic history of snapper. Analyses indicated that haplotype diversity was high (0.968-0.982), which is commonly observed in species with large populations sizes. Mitochondrial genomes showed the presence of two lineages that diverged approximately 650,000 (490,000 – 840,000) years ago. The separation was likely linked to reductions in sea level during glacial cycles. Estimates of changes in population size show strong support for an exponential population size increase after the last glacial maximum (LGM). Changes in population abundance based on the Bayesian Skyline plot indicated a strong population increase approximately 10,000 years ago. The steep increase in new branches in the phylogenetic tree suggests population sizes increase approximately 20,000 (7,000-35,000) years ago. A post-glacial expansion is the most likely explanation for the observed increase in population abundance. During this period, sea levels rose which presumably reconnected fragmented populations, and subsequent increased sea temperatures allowed for southward expansion. Whole-genome sequences from contemporary snapper populations were used to identify genes under selection. Analyses were conducted to detect selection in a single genetic cluster (divergent selection), or both genetic clusters (nation-wide selection). In total, 101 genomic regions containing 253 different genes showed evidence for selection. Two genomic regions showed strong evidence for divergent selection between the northern and southern cluster (FST > 0.2). The regions contained two genes associated with glycolysis which are linked to (cell-) growth (i.e. mast2 and hk2). The regions containing hk2 showed a lack of rare alleles (TD > 2) in the southern cluster, consistent with balancing selection maintaining multiple alleles in the population. Variation in growth rate may be maintained throughout the genetic cluster because of a latitudinal gradient in sea temperature. Strong evidence for selective sweeps were detected in two genomic regions on a nation-wide level. Both regions contained genes associated with angiogenesis (mydgf and rnf213a), which has been shown to affect maturation in species of fish. While tentative, it is possible that intense size-selective fishing is selecting for early maturation in snapper, a life life-history commonly associated with fishing-induced evolution. A selection scan contrasting the population Tasman Bay and Karamea Bight was performed to test for evidence of adaption to cold stress. Selection was detected in 123 genomic regions containing 296 genes, of which 197 potentially experience divergent selection. Two genes were located in regions that showed significant evidence of selection (camk2g and ksr2). Both genes have been associated with cold stress in previous studies, suggesting the Karamea Bight could represent an adaptive front at the southern range of the distribution of snapper. This thesis presents the first population genomic study of Australasian snapper in New Zealand, a species with a diverse genetic landscape and a rich evolutionary history. The detection of fine-scale population structure through adaptive differences between populations highlights the promising application of genomics in fisheries management. The study of mitochondrial lineages showed the effect of glacial cycles, providing insights into how New Zealand’s marine fauna has been affected by major changes in global climate. Finally, the identification of genes and associated biological traits under selection has provided fundamental new insights regarding the environmental conditions that drive adaptive change and act on phenotypes. Snapper is an ideal species for developing and integrating genomics into New Zealand fisheries management. A detailed understanding of fish stock demography and adaptive potential is critical to support improvement to fisheries management as wild stocks continue to face strong anthropogenic pressures (e.g. climate change and overexploitation). Genomics provides valuable insights into how stock assessments and harvesting levels can be better set to match the natural biological units of a species that are determined by gene flow and adaptive variation.

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