Inbreeding and the cougar genome

This week, some of my favorite #scicomm games on Twitter are teaming up with March Mammal Madness to reveal this year’s #2020MMM contestants in my favorite “battle of the fittest.” Specifically, today (2/21/2020) at 12:30 pm EST, Dr. Michelle LaRue (@drmichellelarue) will be dropping an image for her #CougarOrNot science communication game with the big combatant reveal at 2:30 pm EST.

Photo provided by National Parks Service via Wikimedia

The timing is appropriate because the genome of the cougar (Puma concolor; also called mountain lion or puma) was published at the end of last year, providing insights into the divergence between North and South American cougars, as well as some interesting findings regarding genomic diversity that have conservation implications for the puma (Saremi & Supple et al. 2019). Continue reading for some cool cougar insights to prepare you to fill your #2020MMM bracket!

Co-First Authors Nedda F. Saremi (on left) & Megan A. Supple
(Photo credits: Linkedin & UCSC Paleogenomics Lab)

Cougars range from the northern Yukon to the tip of South America, but extensive hunting pressure in the 19th and 20th centuries pushed many populations nearly to extinction in North America and essentially pushed all cougars out of the Midwest and East Coast of North America (although they are returning!), except for subspecies populations of the Florida panther. Since the mid-20th century, cougar populations have increased and recolonized some areas, resulting in some cougar populations being large and well-connected while others are small and fragmented. The Florida panther has been a poster child for classic conservation genetics (e.g., microsatellite genotyping: check out Tears of the Cheetah for a great recap) and genetic rescues (Pimm et al. 2006), but genomic scale data allow us to ask different questions. Saremi and colleagues generated a draft genome for a cougar individual, 36m, from the Santa Cruz Mountains, as well as resequenced nine other individuals from across North and South America (Figure 1).

Figure 1 reproduced from Saremi & Supple et al. 2019

From these genomic data, the most recent common ancestor of the cougars sampled appears to have lived ~300,000 years ago, when cougars from South America dispersed northwards. The cougar population throughout the Americas was largest ~130,000 years ago, but then declined as the climate cooled. The common maternal ancestor of North American pumas appears to have lived ~20,000 years ago, around the peak of the last ice age.

The authors then examined genetic diversity for the sampled populations of cougars in two ways: First, using average genome-wide heterozygosity and second by looking for runs of homozygosity (ROHs). ROHs are long segments of the genome that have homozygous genotypes because an individual inherited the same genotype from each parent. ROH lengths correlate with inbreeding in a population, such that large, mixed populations have shorter ROHs whereas isolated or bottlenecked populations have more frequent and longer ROHs (Ceballos et al. 2017). The two cougars from Brazil (represented in brown in Figure 4) were the least inbred, whereas two Florida panthers from Big Cypress (dark green in Figure 4) before the 1995 genetic rescue were the most inbred. Inbreeding and ROH patterns were consistent with estimated population sizes and histories across all samples. All North American cougars had tracts of ROH, but interestingly the tracts were not identical across populations (Figure 4a). This study illustrated well how heterozygosity can be misleading. For example, one individual (light green dot in Figure 4) from the ‘rescued’ Florida panther population was as heterozygous as the individuals from Brazil, but had large ROH tracts because of its history of admixture from the genetic rescue.

Figure 4 reproduced from Saremi & Supple et al. 2019

Ultimately, this study showed that cougars in isolated North American populations exhibit the genomic consequences of inbreeding, i.e. low heterozygosity and long ROHs. However, because the ROHs from each population differ such that areas of low genetic diversity are not shared between populations, gene flow between populations could restore at least some lost genetic diversity if established by wildlife corridors and translocations. Further, these results foreshadow what even moderate fragmentation might do to larger cougar populations in North and South America, or even to other top predators in which population densities are low and successful migrants infrequent.

Other news coverage: https://news.ucsc.edu/2019/10/puma-genome.html

References:

Ceballos, F., Joshi, P., Clark, D. et al. Runs of homozygosity: windows into population history and trait architecture. Nat Rev Genet 19, 220–234 (2018). https://doi.org/10.1038/nrg.2017.109

Pimm, S.L., Dollar, L., & Bass Jr, O.L. The genetic rescue of the Florida panther. Animal Conserv 9, 115-122 (2006) https://doi.org/10.1111/j.1469-1795.2005.00010.x

Saremi, N.F., Supple, M.A., Byrne, A. et al. Puma genomes from North and South America provide insights into the genomic consequences of inbreeding. Nat Commun 10, 4769 (2019). https://doi.org/10.1038/s41467-019-12741-1

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