Divergence and serial colonization shape genetic variation and define conservation units in Asian elephants

Abstract

Asian elephants (Elephas maximus) are the largest extant terrestrial megaherbivores native to Asia, with 60% of their wild population found in India. Despite ecological and cultural importance, their population genetic structure and diversity, demographic history, and ensuing implications for management/conservation remain understudied. We analyzed 34 whole genomes (between 11× and 32×) from most known elephant landscapes in India and identified five management/conservation units corresponding to elephants in Northern (Northwestern/Northeastern), Central, and three in Southern India. Our data reveal signatures of divergence and serial colonization and a potential dilution of genetic diversity from north to south of India. The northern populations diverged from others more than 70,000 years ago, have higher genetic diversity, and have low inbreeding (pi = 0.0016 ± 0.0001; F_{ROH > 1 MB} = 0.09 ± 0.03). Two of three populations in Southern India have low diversity and are inbred, with very low effective population sizes compared with census sizes (pi = 0.0014 ± 0.00009 and 0.0015 ± 0.0001; F_{ROH > 1 MB} = 0.25 ± 0.09 and 0.17 ± 0.02). Analyses of genetic load reveal the purging of potentially high-effect insertion/deletion (indel) deleterious alleles in the southern populations and a decreasing number of deleterious alleles from north to south in India. However, despite dilution and purging for the damaging mutation load in Southern India, the load that remains is homozygous. High homozygosity of deleterious alleles, coupled with low neutral genetic diversity, make southernmost populations high priority for conservation attention. Most surprisingly, our study suggests that patterns of genetic diversity and genetic load can correspond to genomic signatures of serial founding events, even in large, highly mobile, endangered mammals.

Keywords: South Asia; conservation genomics; elephant management; extinction; genetic load; megaherbivores; serial dilution.