Genomic impact of severe population decline in a nomadic songbird.

Sam Banks,Robert Heinsohn,Dejan Stojanovic,Laura Rayner,Michael A. Russello,Tomasz Suchan,Marcin Adamski,Nicola Aitken,George Olah,Brenton von Takach Dukai,Ross Crates,Dean Ingwersen,Louis Ranjard

doi:10.1371/journal.pone.0223953

Abstract

Uncovering the population genetic histories of non-model organisms is increasingly possible through advances in next generation sequencing and DNA sampling of museum specimens. This new information can inform conservation of threatened species, particularly those for which historical and contemporary population data are unavailable or challenging to obtain. The critically endangered, nomadic regent honeyeater Anthochaera phrygia was abundant and widespread throughout south-eastern Australia prior to a rapid population decline and range contraction since the 1970s. A current estimated population of 250–400 individuals is distributed sparsely across 600,000 km2 from northern Victoria to southern Queensland. Using hybridization RAD (hyRAD) techniques, we obtained a SNP dataset from 64 museum specimens (date 1879–1960), 102 ‘recent’ (1989–2012) and 52 ‘current’ (2015–2016) wild birds sampled throughout the historical and contemporary range. We aimed to estimate population genetic structure, genetic diversity and population size of the regent honeyeater prior to its rapid decline. We then assessed the impact of the decline on recent and current population size, structure and genetic diversity. Museum sampling showed population structure in regent honeyeaters was historically low, which remains the case despite a severe fragmentation of the breeding range. Population decline has led to minimal loss of genetic diversity since the 1980’s. Capacity to quantify the overall magnitude of both genetic diversity loss and population decline was limited by the poorer quality of genomic data derived from museum specimens. A rapid population decline, coupled with the regent honeyeater’s high mobility, means a detectable genomic impact of this decline has not yet manifested. Extinction may occur in this nomadic species before a detectable genomic impact of small population size is realised. We discuss the implications for genetic management of endangered mobile species and enhancing the value of museum specimens in population genomic studies.

Highlights

Large-scale habitat loss and fragmentation is a widespread and ongoing global process [1], affecting the demographics and population genetics of species through altered patterns of dispersal, reproduction and selection [2]
We aimed to quantify the impact of widespread habitat loss on the population genomic structure, diversity and effective population size of the wild regent honeyeater populations over these time periods
To assess the potential for sampling bias to be introduced by lower quality data derived from the museum samples, we evaluated the effect of read depth on genetic diversity measures

Summary

Introduction

Large-scale habitat loss and fragmentation is a widespread and ongoing global process [1], affecting the demographics and population genetics of species through altered patterns of dispersal, reproduction and selection [2]. Species with limited dispersal capacity and short generation times are susceptible to rapid loss of genetic variation within populations, increases in genetic structure among populations and reduced fitness, following habitat fragmentation [4]. Loss or degradation of critical habitat elements is a major risk [8] Alternative population pressures such as harvesting can have major negative impacts [9, 10]. In the case that functional population connectivity is reduced, mobile species may be susceptible to rapid population decline Negative genetic effects such as inbreeding depression can emerge once populations become small or fragmented [4], as rapid population decline limits opportunities to purge deleterious alleles from the population [11]

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