Recent Evolutionary History of Tigers Highlights Contrasting Roles of Genetic Drift and Selection

Abstract

Species conservation can be improved by knowledge of evolutionary and genetic history. Tigers are among the most charismatic of endangered species and garner significant conservation attention. However, their evolutionary history and genomic variation remains poorly known, especially for Indian tigers. With 70% of the worlds wild tigers living in India, such knowledge is critical. We re-sequenced 65 individual tiger genomes representing most extant subspecies with a specific focus on tigers from India. As suggested by earlier studies, we found strong genetic differentiation between the putative tiger subspecies. Despite high total genomic diversity in India, individual tigers host longer runs of homozygosity, potentially suggesting recent inbreeding or founding events, possibly due to small and fragmented protected areas. We suggest the impacts of ongoing connectivity loss on inbreeding and persistence of Indian tigers be closely monitored. Surprisingly, demographic models suggest recent divergence (within the last 20,000 years) between subspecies, and strong population bottlenecks. Amur tiger genomes revealed the strongest signals of selection related to metabolic adaptation to cold, while Sumatran tigers show evidence of weak selection for genes involved in body size regulation. We recommend detailed investigation of local adaptation in Amur and Sumatran tigers prior to initiating genetic rescue.

High frequency of an otherwise rare phenotype in a small and isolated tiger population

“…We studied 599 tigers across the tiger range at the Taqpep c.1360C > T variant site. We genotyped 85 tigers using whole-genome data for four subspecies [Amur, Malayan, and Sumatran: 29, Armstrong et al ( 40 ), and Bengal tigers: 56, Khan et al ( 5 ), Khan et al ( 41 ), Armstrong et al ( 40 ), and this study] and recorded all of them as homozygous for the wild-type allele. We also attempted to PCR amplify the Taqpep c.1360C > T mutation locus ( Methods ) from 528 genetically identified individuals from primarily noninvasive sources [samples from Natesh ( 42 ), Reddy et al ( 43 ), Reddy et al ( 44 ), and ongoing studies in Central India, North, and northeast India].…”

Genomic evidence for inbreeding depression and purging of deleterious genetic variation in Indian tigers

“…Each genetic cluster consists of several protected areas, with varying connectivity with other such protected areas and clusters (Jhala et al 2020, Kolipakam et al 2019, Alcala et al 2019. For the purpose of this paper, we defined populations, and whether they are 'isolated' or 'connected' based on population genetic and gene flow analyses using markers across the genome (Armstrong et al 2021, Natesh et al 2017and Alcala et al 2019. Here, the 'large' populations currently have hundreds of tigers (minimum 300 tigers), while 'small' populations currently have below 100 tigers (Jhala et al 2020).…”

“…from Central India and Northwest), while central large-connected population (Central Indian landscape) was connected by gene flow to other tiger genetic clusters until recently (see Natesh et al 2017 andAlcala et al 2019). SFS-based demographic history models in Armstrong et al (2021) suggest that most Indian tigers diverged from each other recently. Increased agriculture, bounty hunting and illegal poaching, habitat loss and fragmentation together have led to local extinctions of tiger populations (Rangarajan 2005, Sramek 2006).…”

“…We collected tissue from tranquilized or dead tigers from several tiger reserves ( 14protected areas) and a zoo across India (Figure 5, Supplementary Table 1) that belonged to one of five population clusters: 1) Small-isolated population from north-western India (NW) (n=18) -we obtained tissue from 18 NW individuals and used data from two NW individuals in Armstrong et al (2021). Our NW samples consist only of individuals that were born in Ranthambore Tiger Reserve (RTR) but and 0.28 (n=3) (Supplementary Table 1).…”

“…We use Bengal tigers (Panthera tigris tigris) from India as a model to investigate levels of inbreeding and relative mutation loads in small-isolated and largeconnected populations, and examine the potential for genetic rescue. Tigers are large, endangered carnivores, but Bengal tigers have high genetic variation compared to other sub-species, with some sub-populations showing high inbreeding indicating isolation (Armstrong et al 2021). All Bengal tiger populations have been through historic bottlenecks, but inbreeding and genetic variation vary among populations.…”