Wednesday, December 1, 2021

Tigers That Change Their Stripes

Two white tigers, a black tiger and two typically patterned tigers.  Left-to-right:  A leucistic tigress, a leucistic pseudo melanistic tiger, a pseudo melanistic tiger, and two typically patterned tigers.
Photo:  Rajesh Kumar Mohapatura

A subpopulation of big cats with rare coloring shows evolution in action.

Tigers (Panthera tigris) can indeed change their stripes—and in the Similipal Tiger Reserve in eastern India (Bhanjpur, Baripada, Odisha State), many have done just that.  So-called black tigers, genetic mutants that sport unusually wide and merged stripes (pseudo melanistic), were extremely rare even when tigers were plentiful centuries ago.  But in Similipal today, one in three are black.  A study in the Proceedings of the National Academy of Sciences USA, High frequency of an otherwise rare phenotype in a small and isolated tiger population, Sagar et. al. September 28, 2021 PNAS 118(39), pinpoints the peculiar pattern's genetic cause and reveals evolution at work among these endangered cats.

A black tiger in India
Photo:  Rajesh Kumar Mohapatra

After sequencing the genomes of three zoo-born black tigers and their typical-coated parents, researchers at India's National Center for Biological Sciences and their colleagues tracked the pattern to a tiny change in a gene called taqpep

Taqpep is an abbreviation for Transmembrane Aminopeptidase Q.  

They then spent months hiking about 1,500 kilometers of jungles across India, collecting tiger droppings, fur, blood and drool.  Analyzing these samples helped them determine the prevalence of this genetic change—and its virtual absence in tigers outside Similipal.

Weebles-the-cat, pictured here sitting on my keyboard, has a classic tabby Mackerel pattern with stripes running parallel down her sides.  She is also unimpressed with the subject matter of this post.

Altered taqpep genes were already known to cause blotched tabby patterns in cats, as well as king cheetahs' unusually large spots and stripes.  But such large patterns are so rare because they occur only when genes from both parents have matching mutations.
A king cheetah with unusually large spots and stripes

The new study found that 10 out of the 12 Similipal tigers sampled had at least one copy of this particular taqpep change—and four were black tigers, with two copies each.  But remarkably, not one of the 395 tigers surveyed outside the reserve had even one copy of the mutation.  This suggests that the Similipal tigers are so isolated that they never breed with tigers outside that range and that the bgoup has begun to maintain genetic changes over generations.  "It was an astonishing finding," remarks molecular ecologist and lead author Vinay Sagar.
A kitten with a blotched tabby pattern (swirls)

For senior author Uma Ramakrishnan, a molecular ecologist who has studied Indian tigers' diminishing genetic diversity for more than a decade, this finding is "the most exciting discovery" of her career—stark observable evidence of tigers' fragmentation across the region.

The extensive data collected for this research "provide that much needed baseline for further studies on the genetics of endangered tigers," says University of Rochester evolutionary biologist Nancy Chen, who was not involved in the study.  Although it is unknown if the unusual stripes help or harm the Similipal tigers, the markings underscore the fact that these animals are breeding exclusively among themselves—perhaps to their own peril.

Complete 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 pseudo melanistic, characterized by wide, merged stripes. Camera trap data across the tiger range revealed the presence of pseudo melanistic tigers only in Similipal. We investigated the genetic basis for pseudo melanism 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 pseudo melanism co-segregates 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.

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