Genomic insights into the conservation status of the world\u2019s last remaining Sumatran rhinoceros populations

Johanna Von Seth ,Christopher W Wheat ,Stefan Prost ,M Thomas P Gilbert ,Oliver A Ryder ,Shanlin Liu ,Verena E Kutschera ,Anders Götherström ,Nicolás Dussex ,David Díez‐Del‐Molino ,Selina Brace ,Cynthia Steiner ,Katerina Guschanski ,Tom Van Der Valk ,Mikkel‐Holger S Sinding ,Benoît Goossens ,Senthilvel K S S Nathan ,Marcin Kierczak ,Pontus Skoglund ,Yvonne L Chan ,Love Dalén

doi:10.1038/s41467-021-22386-8

Abstract

Small populations are often exposed to high inbreeding and mutational load that can increase the risk of extinction. The Sumatran rhinoceros was widespread in Southeast Asia, but is now restricted to small and isolated populations on Sumatra and Borneo, and most likely extinct on the Malay Peninsula. Here, we analyse 5 historical and 16 modern genomes from these populations to investigate the genomic consequences of the recent decline, such as increased inbreeding and mutational load. We find that the Malay Peninsula population experienced increased inbreeding shortly before extirpation, which possibly was accompanied by purging. The populations on Sumatra and Borneo instead show low inbreeding, but high mutational load. The currently small population sizes may thus in the near future lead to inbreeding depression. Moreover, we find little evidence for differences in local adaptation among populations, suggesting that future inbreeding depression could potentially be mitigated by assisted gene flow among populations.

Highlights

Small populations are often exposed to high inbreeding and mutational load that can increase the risk of extinction
In order to estimate genomic diversity and mutational load in modern and historical populations, we mapped paired-end data from 18 resequenced genomes Sumatran rhinoceros specimens from Sumatra, Borneo and the Malay Peninsula to a de novo assembly reference genome for Sumatran rhinoceros
Consistent with previous analyses of mitogenome data[31], our phylogenetic tree based on pairwise genetic distances and principal component analysis (PCA) revealed three distinct and reciprocally monophyletic clusters corresponding to the Sumatran, Malay Peninsula and Bornean populations (Fig. 1b, Supplementary Fig. 1, Supplementary Table 1; see ‘Methods’)

Summary

Introduction

Small populations are often exposed to high inbreeding and mutational load that can increase the risk of extinction. A growing body of empirical studies on critically endangered species[4,5] indicates that small populations are often exposed to genomic erosion, which reduces species viability via loss of genetic diversity, increase in inbreeding and in genetic load (i.e., decrease in average individual fitness relative to the fittest genotype due to deleterious mutations) through genetic drift[6,7,8] The magnitude of these processes can vary among populations and species due to their different demographic histories (e.g., population fluctuations and founder effects), sensitivity to environmental changes or life-history traits. Concerns over potential disruption of local adaptation has been one of the main reasons why assisted gene flow has only rarely been used in conservation biology (~34 studies[19])

Objectives

Methods

Results

Conclusion