New revelations of tiger genomes
Tiger genomes reveal signatures of population bottlenecks, recent divergence between subspecies, local adaptation, and ongoing impacts of fragmentation
IMAGE: RANTHAMBORE TIGER view more
CREDIT: RANTHAMBORE TIGER TEAM, NCBS
Genetic variation is like money in the bank: the more you have, the better your chances of survival in the future. Population bottlenecks decrease genetic variation, especially in endangered species. An individual's genome comprises the events that have impacted genetic variation over time, and relatively recent sequencing technologies allow us to read and interpret genetic variation across the genome. Although tigers have received significant conservation attention, little is known about their evolutionary history and genomic variation. This is especially true for Indian tigers, and with 70% of the world's tigers living in India, such understanding is critical to tiger conservation.
A team of researchers from the National Centre for Biological Sciences (NCBS), Stanford University, and zoological parks and NGOs across the world recently completed a three-year project to gain insights into genomic variation in tigers and the processes that have sculpted it. The work, just published in Molecular Biology and Evolution, reiterates that tiger subspecies are genetically distinct and reveals that although Indian tigers have the highest total genetic variation, some individuals are inbred. Simulations based on the genomic data suggest relatively recent divergences between subspecies, and intense population bottlenecks. Analyses also indicate adaptation to cold environments in Russian far east tigers, and potential selection on body size in Sumatran tigers.
The team sequenced whole genomes from 65 individual tigers from four subspecies, with a specific aim to enhance genomes from wild tigers in different habitats in India. They used these data to conduct a variety of population genomic analyses that quantify genetic variability, and investigate the partitioning of genetic variation, possible impacts of inbreeding and founder events, demographic history (including population divergence) and possible signatures of local adaptation.
They found that total genomic variation in Indian tigers was higher than in other subspecies. However, several individual tigers in India had low variation, suggesting possible inbreeding and founding bottlenecks. Tigers from northeast India were the most divergent/different from other populations in India. "Given our results, it is important to understand why some Bengal tigers appear inbred and what the consequences of this are," says Anubhab Khan, co-first author, NCBS.
The history of tiger populations from across their current range shows recent divergences between tiger subspecies, within the last 20,000 years, which is concordant with a transition from glacial to interglacial climate change and increasing human impacts across Asia. These findings are in sharp contrast to an earlier study by ShuJin Luo and others in 2018 that suggested much older divergence times. The recent divergence between populations will need to be investigated further with expanded datasets and analyses of more tiger genomes.
The data and analyses also suggest strong bottlenecks in all tiger populations, highlighting the importance of population size decline on the erosion of genetic variation. "Most studies focusing on species of conservation concern use limited numbers of specimens to try to gain understanding into how genomic variation is partitioned. It is clear from our work here, and a growing number of other studies, that it is crucial to increase our sampling efforts and use caution when interpreting results from limited sample sizes," comments Ellie Armstrong, co-first and co-corresponding author, Stanford University.
Genomes of tigers in the Russian far east suggest adaptation to the cold, while those of Sumatran tigers suggest selection based on body size. Co-senior author Elizabeth Hadly of Stanford University says, "The tiger is an excellent example of the myriad historic events that sculpt species' genomic diversity and points to the importance of understanding this diversity as we attempt to stave off extinction of our most precious species on Earth. While some populations demonstrate the importance of adaptation to local conditions, other evidence suggests that particular populations may suffer the effects of climatic change in the Anthropocene." Such information will be critical to the success of genetic rescue efforts, which should take local adaptation into consideration.
'I have worked on Indian tiger genetic variation for over a decade and always wondered how they compared to other wild tigers. Our study reveals that while the total variation in Indian tiger genomes is high, they have also been dramatically shaped by population bottlenecks. The genomic variation of Indian tigers continues to be shaped by the ongoing loss of connectivity. Population management and conservation action must incorporate information on genetic variation. I hope doing so will help India maintain the gains in tiger conservation achieved so far,' says Uma Ramakrishnan, co-senior and co-corresponding author, NCBS.
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https:/Increasingly fragmented tiger populations may require 'genetic rescue'
Despite being one of the world's most charismatic species, tigers face uncertain futures primarily due to habitat fragmentation, human-wildlife conflict and poaching. As global tiger populations decline, so does their genetic diversity. But until now it's been unclear how the animals' dwindling numbers are affecting them at the genetic level.
To find out, researchers at Stanford University, the National Centre for Biological Sciences, India, and various zoological parks and NGOs sequenced 65 genomes from four of the surviving tiger subspecies. Their findings confirmed that strong genetic differences exist between different tiger subspecies but showed, surprisingly, that these differences emerged relatively recently, as Earth underwent a major climatic shift and our own species grew increasingly dominant.
The research, detailed in a new paper published this week in the journal Molecular Biology and Evolution, shows how genomics can help guide conservation efforts toward wild tigers and other species, said study co-leader Elizabeth Hadly, the Paul S. and Billie Achilles Professor in Environmental Biology in the School of Humanities and Sciences.
"The increasing dominance of humans across the world means that our understanding of which attributes of species and populations are best suited to the Anthropocene becomes ever more important," said Hadly, referring to the proposed geological epoch marked by significant human impact on the environment.
"Some populations are well adapted to a future dominated by humans and our new climates and others are not, so any type of management of species should be informed by what we can glean from their genomes," added Hadly, who is also a senior fellow at the Stanford Woods Institute for the Environment. "Conservation genomics is far from a perfect science, but this tiger study hints at the power of adequate sampling across both the species range and its genome."
The study reveals that the world's existing tiger subspecies began exhibiting signs of dramatic and recent contractions starting only around 20,000 years ago - a period that coincided with both the global transition out of the Pleistocene Ice Age and the rise of human dominance in Asia. Each subspecies of tiger the team studied showed unique genomic signatures as a consequence of their increasing isolation from one another.
For example, local environmental genomic adaptation to cold temperatures was found in the Siberian (or Amur) tigers, the northernmost tigers found in the Russian Far East. These adaptations were absent in the other tiger subpopulations studied. Tigers from Sumatra, meanwhile, showed evidence of adaptations for body size regulation, which could help explain their overall smaller size. Despite these adaptations, tigers from these populations have low genetic diversity, suggesting that if populations continue to decline, genetic rescue may need to be considered.
One form that rescue might take is through the mating of different tiger subspecies together as a way of increasing their genetic diversity and protecting against the ill effects of inbreeding. Inbreeding occurs when populations are so small and isolated from other populations that related individuals breed with each other. Over time, this leads to lower genomic diversity and to the emergence of recessive diseases, physical deformities and fertility problems that often result in behavioral, health and population declines. Although increasing genetic diversity is one goal, another might be to select for inherited traits that confer higher survival in a changing world.
Even Bengal tigers from India, which comprise about 70 percent of the world's wild tigers and exhibit relatively high genomic diversity compared to other subspecies, showed signs of inbreeding in some populations, the study concluded.
"Some Bengal tiger populations are essentially small islands surrounded by an inhospitable sea of humanity. These tigers cannot disperse and so have only their close relatives to choose as mates," Hadly said.
While many studies investigating endangered species using genomics sequences from a single or just a few individuals, this work reiterates that individuals are not likely to be representative of a population or species status. Further work investigating the consequences of potential inbreeding and diversity declines across the subspecies are needed.
"As genomics has become available to conservation, it is apparent that collaborative studies to investigate the diversity within species are critical," said study first author Ellie Armstrong, a Stanford PhD student in Hadly's lab. "Inferences made from single genomes, while excellent additions to our knowledge of diversity in general, cannot be extrapolated to entire species, especially when using captive animals to infer adaptation to complex habitat change."
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Other Stanford co-authors on the study, titled "Recent Evolutionary History of Tigers Highlights Contrasting Roles of Genetic Drift and Selection," include former postdoctoral scholars Ryan Taylor and Stefan Prost; PhD students Jonathan Kang and Sergio Redondo; Gregory Barsh, professor of genetics and pediatrics, emeritus; Dmitri Petrov, professor of biology; and Christopher Kaelin, staff geneticist.
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