Wild pedigrees inform mutation rates and historic abundance in baleen whales

Abstract

Phylogeny-based estimates suggesting a low germline mutation rate (μ) in baleen whales have influenced research ranging from assessments of whaling impacts to evolutionary cancer biology. We estimated μ directly from pedigrees in four baleen whale species for both the mitochondrial control region and nuclear genome. The results suggest values higher than those obtained through phylogeny-based estimates and similar to pedigree-based values for primates and toothed whales. Applying our estimate of μ reduces previous genetic-based estimates of preexploitation whale abundance by 86% and suggests that μ cannot explain low cancer rates in gigantic mammals. Our study shows that it is feasible to estimate μ directly from pedigrees in natural populations, with wide-ranging implications for ecological and evolutionary research.

The Evolutionary History of Baleen Whales in The Genome Era

“…In the North Atlantic, our pre-whaling NE translated into abundance approximately nine times lower (~ 40,000 individuals) than earlier single locus genetic estimates (Roman & Palumbi, 2003) 360,000 individuals, (Roman & Palumbi, 2003). Our recent demographic results were generally consistent with prewhaling population estimates based on historical records or pedigree-based mutation rates (Sergeant, 1977;Suárez-Menéndez et al, 2023). However, the results here are sensitive recombination and mutation rates, as well as generation time (Kardos et al, 2017).…”

“…Pre-whaling abundance has been the subject of considerable interest and debate as the degree of endangerment of contemporary baleen whale populations is scaled against the historic abundance (Roman & Palumbi, 2003;Suárez-Menéndez et al, 2023;Tulloch et al, 2018;Zerbini et al, 2019). The whole-genome LD-based approach employed in this study suggested that whaling reduced the abundance of the two species in this specific population by 97-98%, confirming the devastating effects of the mechanized, highly effective industrial whaling operations in the Southern Ocean (Rocha, Jr. et al, 2015;Zerbini et al, 2019).…”

“…and precise estimates compared to studies based on a few, potentially unrepresentative, loci (Allendorf et al, 2010). Most importantly, whole genome sequences have enabled the pursuit of new venues of research that have been impossible (or more expensive) before the genome era, such as; assessments of structural genome rearrangements, recombination, pedigree-based mutation rates, linkage of genomic regions, selection, etc (e.g., Allendorf et al, 2010;Henn et al, 2015;Suárez-Menéndez et al, 2023;Theissinger et al, 2023;Waples et al, 2016).…”

“…While genome-based data offer excellent opportunities for phylogenetic and population genetics studies, the most exciting feature of the genome era is that it is now feasible and affordable to access changes in the structure and composition across an entire genome. Comparisons of genome-wide adaptive and detrimental variance (Bertorelle et al, 2022), homozygosity levels (McQuillan et al, 2008), de novo mutations (Bergeron et al, 2023;Conrad et al, 2011;Suárez-Menéndez et al, 2023), and changes in the genomic architecture of wild genomes (Edelman et al, 2019;Fry et al, 2020) are paving the way for novel insights and testing old hypotheses. In a manner, such comparisons serve as natural experiments with which we can empirically assess expectations of population genetic theory in terms of how evolution shapes genetic variance.…”

“…Input files were created using the vcf2smc tool using only derived variants (see polarisation methods in SI Appendix SM3.3). Estimates were performed using the SMC++ estimate, assuming a mutation rate of 1.17 x 10 -8 per generation (Suárez-Menéndez et al, 2023) and time-scaled to generations of 26 years (Taylor et al, 2007). A total of 100 Independent runs were conducted for each population in 20 EM interactions and a threshold tolerance of 1 x 10 -4 .…”