Significant loss of mitochondrial diversity within the last century due to extinction of peripheral populations in eastern gorillas

Abstract

Species and populations are disappearing at an alarming rate as a direct result of human activities. Loss of genetic diversity associated with population decline directly impacts species’ long-term survival. Therefore, preserving genetic diversity is of considerable conservation importance. However, to assist in conservation efforts, it is important to understand how genetic diversity is spatially distributed and how it changes due to anthropogenic pressures. In this study, we use historical museum and modern faecal samples of two critically endangered eastern gorilla taxa, Grauer’s (Gorilla beringei graueri) and mountain gorillas (Gorilla beringei beringei), to directly infer temporal changes in genetic diversity within the last century. Using over 100 complete mitochondrial genomes, we observe a significant decline in haplotype and nucleotide diversity in Grauer’s gorillas. By including historical samples from now extinct populations we show that this decline can be attributed to the loss of peripheral populations rather than a decrease in genetic diversity within the core range of the species. By directly quantifying genetic changes in the recent past, our study shows that human activities have severely impacted eastern gorilla genetic diversity within only four to five generations. This rapid loss calls for dedicated conservation actions, which should include preservation of the remaining peripheral populations.

Historical Genomes Reveal the Genomic Consequences of Recent Population Decline in Eastern Gorillas

“…10,000 years ago [21]. Subsequently, Grauer's gorillas went through a period of population growth and range expansion 5,000-10,000 years ago [22,23]. This demographic expansion may have led not only to a historically higher genetic diversity in Grauer's compared to mountain gorillas ( Figure 2) but also to a higher number of low-frequency deleterious mutations in the Grauer's gorilla population [24,25].…”

“…As Grauer's gorillas went through a severe population decline of 80% in the last 20 years to less than 4,000 individuals today [26], these deleterious mutations appear to have increased in frequency, likely due to increased drift and inbreeding ( Figure 2), thus leading to a more pronounced change in genetic load in Grauer's compared to mountain gorillas (Figure 3). In contrast, the population size of mountain gorillas from the Virunga Massif population has likely remained small since their divergence from the Grauer's gorillas [22,23]. Numbering fewer than 1,000 individuals at least since the late 1950s [27], mountain gorillas experienced a population low of $250 individuals in the 1980s [28] but recovered to $450 individuals in 2013 [29].…”

A roadmap to mammalian oral microbiome evolution with dental calculus

“…We were also able to recover complete mitochondrial genomes (>1X average coverage per site) for one gorilla, three reindeer and two bear samples. Mitochondrial genomes provide a rich source of information about the host evolutionary history, host population structure and changes in host population sizes over time 18,50 . With deeper metagenomics sequencing and/or employment of target capture techniques, the relatively high proportion of host reads allows for investigations into the importance of host genetic diversity and demography in shaping microbiome composition from the same dental calculus sample.…”

“…While the focus to date has been on human-microbiome and human-pathogen co-evolution, many other mammals produce dental calculus. Collections in natural history museums provide the opportunity to study the effects of human-driven changes in animal populations over the last 200 years, including population declines and the introduction of pollutants like antibiotics [17][18][19][20] . Few studies to date have investigated microbiome changes in modern wild animal populations [21][22][23] , and historical populations remain virtually unexplored.…”

Population genomics through time provides insights into the consequences of decline and rapid demographic recovery through head‐starting in a Galapagos giant tortoise

“…Previously, there were few examples of direct investigations of changes in genetic variation in natural populations before and after a known bottleneck event. When studies employed temporally spaced sampling, they typically relied on a limited number of genetic markers to characterize population-level patterns of genetic diversity (e.g., a fragment of the mitochondrial DNA control region and/or 5-24 microsatellite loci; Bouzat, Lewin, & Paige, 1998;Eldridge et al, 2004;Miller & Waits, 2003;Nyström, Angerbjörn, & Dalén, 2006;Ugelvig, Nielsen, Boomsma, & Nash, 2011;Wisely, Buskirk, Fleming, McDonald, & Ostrander, 2002). In recent years, however, there are a growing number of temporal studies investigating bottlenecks using full mitochondrial genome sequences (e.g., Dussex, von Seth, Robertson, & Dalén, 2018;Jensen et al, 2018;van der Valk et al, 2018) and genome-wide markers (e.g., Der Sarkissian et al, 2015;Mikheyev, Tin, Arora, & Seeley, 2015).…”