Historical population declines prompted significant genomic erosion in the northern and southern white rhinoceros (Ceratotherium simum)

Abstract

Large vertebrates are extremely sensitive to anthropogenic pressure, and their populations are declining fast. The white rhinoceros (Ceratotherium simum) is a paradigmatic case: this African megaherbivore suffered a remarkable population reduction in the last 150 years due to human activities. The two white rhinoceros subspecies, the northern (NWR) and the southern white rhinoceros (SWR), however, underwent opposite fates: the NWR vanished quickly after the onset of the decline, while the SWR recovered after a severe bottleneck. Such demographic events are predicted to have an erosive effect at the genomic level, in connection with the extirpation of diversity, and increased genetic drift and inbreeding. However there is currently little empirical data available that allows us to directly reconstruct the subtleties of such processes in light of distinct demographic histories. Therefore to assess these effects, we generated a whole-genome, temporal dataset consisting of 52 re-sequenced white rhinoceros genomes, that represents both subspecies at two time windows: before and during/after the bottleneck. Our data not only reveals previously unknown population substructure within both subspecies, but allowed us to quantify the genomic erosion undergone by both, with post-bottleneck white rhinoceroses harbouring significantly fewer heterozygous sites, and showing higher inbreeding coefficients than pre-bottleneck individuals. Moreover, the effective population size suffered a decrease of two and three orders of magnitude in the NWR and SWR respectively, due to the recent bottleneck. Our data therefore provides much needed empirical support for theoretical predictions about the genomic consequences of shrinking populations, information that is relevant for understanding the process of population extinction. Furthermore, our findings have the potential to inform management approaches for the conservation of the remaining white rhinoceroses.

Complex population structure of the Atlantic puffin revealed by whole genome analyses

“…Nucleotide diversity ( π ) of puffins is significantly different between colonies, with the Spitsbergen population having significantly lower nucleotide diversity than the global median (Wilcoxon Rank Sum test, U = 4824, n SPI = 25, n Global = 300, p < 0.05, Table S5). Colonies also differ significantly in levels of heterozygosity (Kruskal-Wallis Test, p < 0.001; Figure 3a) and inbreeding (Kruskal-Wallis Test, p < 0.001, Figure 3b), whereby individual inbreeding (F RoH ) was approximated based on Runs of Homozygosity (RoH) 39 . Again, the Spitsbergen colony has significantly lower levels of heterozygosity (0.00220 - 0.00223) and significantly higher levels of F RoH values (0.161 - 0.172), compared to the Faroese and Icelandic colonies (Dunn test with Holm correction, p < 0.05).…”

“…We defined the 10% quantile of the average local heterozygosity across all samples as the cutoff for a “low heterozygosity region”. RoHs were declared as all regions with at least two subsequent windows of low heterozygosity (below cutoff) and their final length was calculated as described in Sánchez-Barreiro et al (2020) 39 . We calculated an individual inbreeding coefficient based on the RoH, F RoH , as in Sánchez-Barreiro et al (2020) 39 by computing the fraction of the entire genome falling into RoHs, with the entire genome being the total length of windows scanned.…”

“…The proportion of runs of homozygosity (RoH) within each puffin genome was computed by calculating local estimates of heterozygosity in 100 kbp sliding windows (50 kbp slide) following the approach in Sánchez-Barreiro et al (2020) 39 . We defined the 10% quantile of the average local heterozygosity across all samples as the cutoff for a "low heterozygosity region".…”

A review of UMAP in population genetics

“…UMAP has also been successfully used with ancient DNA samples combined with modern and contemporary populations to identify shared population structure [15], as well as animal populations to study spatial introgression in mussels [16], genetic bottlenecks in the white rhino population [17], and the geographic origin of disease-carrying mosquitoes [18,19].…”

Spatial variation in population genomic responses to over a century of anthropogenic change within a tidal marsh songbird

“…Historical DNA isolated from museum specimens has proven to be a critical resource for establishing baseline levels of genetic diversity and population structure (Wanderler et al 2007). More recent analyses have increasingly leveraged genomic datasets with dramatically increased power to address a host of conservation genetics questions (Bi et al 2013; Suchan et al 2016; Bi et al 2019; Feng et al 2019; van der Valk et al 2019; Sánchez-Barreiro et al 2021). In particular, studies comparing patterns of temporal change at both neutral loci and loci potentially under selection can provide further insights into: (1) how populations adapt to human-mediated ecological change; and (2) how changing patterns of gene flow, population size, and habitat degradation influence variation at neutral versus functional loci.…”