Genomic signatures of population bottleneck and recovery in Northwest Atlantic pinnipeds

Abstract

Population increases over the past several decades provide natural settings in which to study the evolutionary processes that occur during bottleneck, growth, and spatial expansion. We used parallel natural experiments of historical decline and subsequent recovery in two sympatric pinniped species in the Northwest Atlantic, the gray seal (Halichoerus grypus atlantica) and harbor seal (Phoca vitulina vitulina), to study the impact of recent demographic change in genomic diversity. Using restriction site‐associated DNA sequencing, we assessed genomic diversity at over 8,700 polymorphic gray seal loci and 3,700 polymorphic harbor seal loci in samples from multiple cohorts collected throughout recovery over the past half‐century. Despite significant differences in the degree of genetic diversity assessed in the two species, we found signatures of historical bottlenecks in the contemporary genomes of both gray and harbor seals. We evaluated temporal trends in diversity across cohorts, as well as compared samples from sites at both the center and edge of a recent gray seal range expansion, but found no significant change in genomewide diversity following recovery. We did, however, find that the variance and degree of allele frequency change measured over the past several decades were significantly different from neutral expectations of drift under population growth. These two cases of well‐described demographic history provide opportunities for critical evaluation of current approaches to simulating and understanding the genetic effects of historical demographic change in natural populations.

Informing conservation strategies with museum genomics: Long‐term effects of past anthropogenic persecution on the elusive European wildcat

“…Further, long‐lived species may be able to preserve genetic diversity over shorter periods of decline (Hailer et al, 2006 ; Johnson et al, 2008 ; White et al, 2014 ). Various methods exist for the detection of bottlenecks, ranging from classical tests for loss of heterozygosity and changes in allele distribution frequencies to more recent approaches based on genomic data (Allendorf, 2017 ; Cammen et al, 2018 ; Luikart et al, 1998 ). All of these methods rely on a series of assumptions and models, such as a model and rate for mutations, absence of gene flow, mutation‐drift equilibrium before decline, or uniformity of reproductive success (Gattepaille et al, 2013 ; Hoban, Mezzavilla, et al, 2013 ).…”

“…Nevertheless, to increase statistical power for the monitoring of genetic erosion in subsequent studies and reduce potential effects of ascertainment bias, we recommend to aim for a higher number of SNP markers (min. several hundred; e.g., Cammen et al, 2018 ; Ewart et al, 2019 ; Stronen et al, 2019a ), consider second‐generation sequencing of microsatellites (Curto et al, 2019 ), or data from WGS (Larsson et al, 2019 ; Loog et al, 2020 ; White et al, 2018 ).…”

Emergence and radiation of distemper viruses in terrestrial and marine mammals

“…For example, PDV was probably carried to European seal populations by harp seals forced southward during periods of overfishing and collapse of Barents Sea capelin (Mallotus villotus) stocks in 1985-1989 and 2003-2006 [61]. In contrast to the large population sizes of Arctic seals, continental European and North American grey and harbour seal populations have been severely depleted by centuries of hunting up until the implementation of conservation and management measures starting in the 1960s and 1970s [62][63][64]. Thus, up until the late twentieth century, these seal populations have probably been too small and too fragmented to sustain endemic circulation or suffer largescale PDV outbreaks.…”

The reconstruction of invasion histories with genomic data in light of differing levels of anthropogenic transport

“…HTS has been used to reconstruct invasion histories [16,25,26], inferring the presence of multiple and sequential introductions [27,28], as well as revealing the presence of genetic admixture that may have fitness consequences on colonizing populations [25,29]. In addition, studies of neutral loci have analysed population genomic patterns of NIS in both introduced and native ranges [30,31], identified secondary contacts [32] and detected genetic bottlenecks [33]. However, no study using HTS has to date tested how anthropogenic transport of species affects our ability to infer colonization pathways of NIS [26].…”