Serial colonization shapes genetic variation and defines conservation units in Asian elephants

Abstract

Megaherbivores are primary consumers who provide unique ecosystem services. Given their body size, they are disproportionately threatened in the Anthropocene. Asian elephants are the largest extant terrestrial megaherbivores native to Asia, with 60% of the population found in India. Despite their ecological and cultural importance, the management/conservation units, genetic history, diversity and threats remain understudied. We re-sequenced 31 whole genomes (between 11X - 32X) from all known elephant landscapes in India, and identified five management/conservation units corresponding to elephants in northern India, central India and three in southern India. The genetic data reveal signatures of serial colonisation, and a dilution of diversity from north to south of India. The northern populations diverged from other populations more than 70,000 years ago, and have the highest genetic diversity, with low inbreeding/high effective size (Pi = 0.39, SD:0.2; FROH> 1MB= 0.09, SD:0.03). Two of three populations in southern India have low diversity and are inbred with much lower effective sizes than current populations sizes (Pi = 0.25, SD:0.29 and 0.29, SD:0.23; FROH> 1MB= 0.25, SD:0.09 and 0.17, SD:0.02). Additionally, future generations are expected to be more inbred since pairs of extant elephants have large tracts of the genome that are already identical. Analyses of genetic load reveals purging of potentially high-effect deleterious alleles in the southern populations and potential dilution of all deleterious alleles from north to south in India. However, southern Indian elephants are highly homozygous for all the deleterious alleles that persist, despite dilution and purging. High homozygosity of deleterious alleles, coupled with low neutral genetic diversity make them high priority for conservation and management attention. Most surprisingly, our study suggests that patterns of genetic diversity and genetic load can correspond to geographic signatures of serial founding events even in large mobile endangered species.

Population genetics of animals in the wild to aid conservation: Uma Ramakrishnan—Recipient of the 2023 Molecular Ecology Prize

“…Twenty‐five years after starting her first attempt at field ecology on elephants, she returned to the species, using modern genomic techniques to examine population structure with signatures of high inbreeding in small isolated populations (Khan et al., 2023). The motivation to focus on wild animals with conservation implications, like tigers, lions and elephants, is very clear.…”