High frequency of an otherwise rare phenotype in a small and isolated tiger population
Edited by Stephen J O'Brien, Nova Southeastern University, Fort Lauderdale, FL, and approved July 9, 2021 (received for review December 9, 2020)
Commentary
October 7, 2021
Significance
Small and isolated populations have low genetic variation due to founding bottlenecks and genetic drift. Few empirical studies demonstrate visible phenotypic change associated with drift using genetic data in endangered species. We used genomic analyses of a captive tiger pedigree to identify the genetic basis for a rare trait, pseudomelanism, in tigers. Genome sequencing and extensive genotyping of noninvasive samples across tiger range revealed unique spatial presence of this allele in the Similipal Tiger Reserve, India. Population genetic analyses confirmed that Similipal is a small and isolated population. Simulations suggest that intense founding bottlenecks could result in the observed patterns, implicating drift. Our study highlights ongoing phenotypic evolution, potentially from human-induced fragmentation, in endangered large carnivore populations.
Abstract
Most endangered species exist today in small populations, many of which are isolated. Evolution in such populations is largely governed by genetic drift. Empirical evidence for drift affecting striking phenotypes based on substantial genetic data are rare. Approximately 37% of tigers (Panthera tigris) in the Similipal Tiger Reserve (in eastern India) are pseudomelanistic, characterized by wide, merged stripes. Camera trap data across the tiger range revealed the presence of pseudomelanistic tigers only in Similipal. We investigated the genetic basis for pseudomelanism and examined the role of drift in driving this phenotype's frequency. Whole-genome data and pedigree-based association analyses from captive tigers revealed that pseudomelanism cosegregates with a conserved and functionally important coding alteration in Transmembrane Aminopeptidase Q (Taqpep), a gene responsible for similar traits in other felid species. Noninvasive sampling of tigers revealed a high frequency of the Taqpep p.H454Y mutation in Similipal (12 individuals, allele frequency = 0.58) and absence from all other tiger populations (395 individuals). Population genetic analyses confirmed few (minimal number) tigers in Similipal, and its genetic isolation, with poor geneflow. Pairwise FST (0.33) at the mutation site was high but not an outlier. Similipal tigers had low diversity at 81 single nucleotide polymorphisms (mean heterozygosity = 0.28, SD = 0.27). Simulations were consistent with founding events and drift as possible drivers for the observed stark difference of allele frequency. Our results highlight the role of stochastic processes in the evolution of rare phenotypes. We highlight an unusual evolutionary trajectory in a small and isolated population of an endangered species.
Data Availability
Raw sequence data have been deposited in NCBI (Bioproject accession no. PRJNA749163). Previously published data were used for this work (https://doi.org/10.1093/molbev/msab032, https://doi.org/10.1002/ece3.6157, and https://doi.org/10.1101/2021.05.18.444660). Scripts for variant calling and filtering, population genetics simulations, and datasheets are available from Github (https://doi.org/10.5281/zenodo.5244876).
Acknowledgments
We sincerely thank the NTCA (NTCA permit 15-30(10)/2015-NTCA), CZA (CZA permit 9-3/2005-CZA(Vol lll)(D)/694/2017), OSFD (OSFD permits 1057/4 WL-579/2017, 11472/4 WL-579/2017, and 489/4 WL-579/2017), Madhya Pradesh Forest Department (permit No./Tech-1/2048 and No./Tech-1/7661), Tamil Nadu Forest Department (permit 3789/2019/WL1), Uttarakhand Forest Department (permit 90/5-6), Uttar Pradesh Forest Department (permit 1127/23-2-12(G) and 1891/23-2-12), and Bihar Forest Department (permit Wildlife-589) for permissions; Nandankanan Zoological Park (permit 6423/4 WL-579/2017), Bhubaneswar, Arignar Anna Zoological Park (permit 3789/2019/WL1), Chennai, Advanced Institute for Wildlife Conservation, Chennai, Odisha University of Agriculture & Technology, Bhubaneswar, and Anubhab Khan, Aditi Patil, and B. V. Aditi Prasad for tiger samples; OSFD staff at the Similipal Tiger Reserve (especially Maloth Mohan, Amitabh Brahma, and J. D. Pati) for support during the field work; Abishek Harihar for help with the field planning and simulations; Awadhesh Pandit, National Centre for Biological Sciences (NCBS) Sequencing Facility, and Anup Chugani, Medgenome, for sequencing; and Jay Storz, Trevor Price, Marty Kardos, V. V. Robin, Shomita Mukherjee, Megan Aylward, and Anubhab Khan for critical comments on the manuscript. Comments from three anonymous referees and the handling editor significantly improved this manuscript. V.S. was supported by the NCBS/Tata Institute of Fundamental Research (TIFR) (Department of Atomic Energy), M.N. and Western Ghats sampling/labwork were supported by a Department of Biotechnology (DBT), India grant (BT/PR13854/BCE/8/809/2010) to U.R., and H.C. was supported by a DBT Wellcome India Alliance grant to U.R. (IA/S/16/2/502714). The NCBS data cluster used is supported under project 12-R&D-TFR-5.04-0900, Department of Atomic Energy, Government of India. This work was supported by the NTCA grant (15-30(10)/2015-NTCA) to U.R., DBT Wellcome Trust India Alliance Senior award to U.R. (IA/S/16/2/502714), and the NCBS/TIFR internal plan fund awarded to U.R. (Project Identification RTI 4006, Department of Atomic Energy, Government of India).
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Cover image: Pictured is an embryo of Xenopus tropicalis immunostained to visualize the epidermal multiciliated cells (yellow/red) and convoluted embryonic kidney tubule (cyan). Maike Getwan et al. modeled skeletal ciliopathies, which are often associated with cystic kidney disease, by using CRISPR to mutate two disease genes in X. tropicalis froglets. Targeting the gene ttc30α recapitulated skeletal malformations and renal cysts typically seen in patients, suggesting that the proteins TTC30A/B are essential for ciliary segmentation, cartilage differentiation, and renal tube formation. The findings may inform the development of novel therapies for ciliary skeletopathies and cystic kidney disease. See the article by Getwan et al., e2106770118. Image credit: Soeren S. Lienkamp.
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Copyright © 2021 the Author(s). Published by PNAS. This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY).
Data Availability
Raw sequence data have been deposited in NCBI (Bioproject accession no. PRJNA749163). Previously published data were used for this work (https://doi.org/10.1093/molbev/msab032, https://doi.org/10.1002/ece3.6157, and https://doi.org/10.1101/2021.05.18.444660). Scripts for variant calling and filtering, population genetics simulations, and datasheets are available from Github (https://doi.org/10.5281/zenodo.5244876).
Submission history
Accepted: July 9, 2021
Published online: September 13, 2021
Published in issue: September 28, 2021
Keywords
Acknowledgments
We sincerely thank the NTCA (NTCA permit 15-30(10)/2015-NTCA), CZA (CZA permit 9-3/2005-CZA(Vol lll)(D)/694/2017), OSFD (OSFD permits 1057/4 WL-579/2017, 11472/4 WL-579/2017, and 489/4 WL-579/2017), Madhya Pradesh Forest Department (permit No./Tech-1/2048 and No./Tech-1/7661), Tamil Nadu Forest Department (permit 3789/2019/WL1), Uttarakhand Forest Department (permit 90/5-6), Uttar Pradesh Forest Department (permit 1127/23-2-12(G) and 1891/23-2-12), and Bihar Forest Department (permit Wildlife-589) for permissions; Nandankanan Zoological Park (permit 6423/4 WL-579/2017), Bhubaneswar, Arignar Anna Zoological Park (permit 3789/2019/WL1), Chennai, Advanced Institute for Wildlife Conservation, Chennai, Odisha University of Agriculture & Technology, Bhubaneswar, and Anubhab Khan, Aditi Patil, and B. V. Aditi Prasad for tiger samples; OSFD staff at the Similipal Tiger Reserve (especially Maloth Mohan, Amitabh Brahma, and J. D. Pati) for support during the field work; Abishek Harihar for help with the field planning and simulations; Awadhesh Pandit, National Centre for Biological Sciences (NCBS) Sequencing Facility, and Anup Chugani, Medgenome, for sequencing; and Jay Storz, Trevor Price, Marty Kardos, V. V. Robin, Shomita Mukherjee, Megan Aylward, and Anubhab Khan for critical comments on the manuscript. Comments from three anonymous referees and the handling editor significantly improved this manuscript. V.S. was supported by the NCBS/Tata Institute of Fundamental Research (TIFR) (Department of Atomic Energy), M.N. and Western Ghats sampling/labwork were supported by a Department of Biotechnology (DBT), India grant (BT/PR13854/BCE/8/809/2010) to U.R., and H.C. was supported by a DBT Wellcome India Alliance grant to U.R. (IA/S/16/2/502714). The NCBS data cluster used is supported under project 12-R&D-TFR-5.04-0900, Department of Atomic Energy, Government of India. This work was supported by the NTCA grant (15-30(10)/2015-NTCA) to U.R., DBT Wellcome Trust India Alliance Senior award to U.R. (IA/S/16/2/502714), and the NCBS/TIFR internal plan fund awarded to U.R. (Project Identification RTI 4006, Department of Atomic Energy, Government of India).
Notes
This article is a PNAS Direct Submission.
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Competing Interests
The authors declare no competing interest.
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