Neo-sex chromosomes and demography shape genetic diversity in the Critically Endangered Raso Lark

Abstract

Generally small effective population sizes expose island species to inbreeding and loss of genetic variation. The Raso lark has been restricted to a single islet for ~500 years, with a population size of a few hundred. To investigate the factors shaping genetic diversity in the species, we assembled a reference genome for the related Eurasian skylark and then assessed genomic diversity and demographic history using RAD-seq data (26 Raso lark samples and 52 samples from its two most closely related mainland species). Genetic diversity in the Raso lark is lower than in its mainland relatives, but is nonetheless considerably higher than anticipated given its recent population size. We found that suppressed recombination on large neo-sex chromosomes maintains divergent alleles across 13% of the genome in females, leading to a two-fold increase in overall diversity in the population. Moreover, we infer that the population contracted from a much larger size recently enough, relative to the long generation time of the Raso lark, that much of the pre-existing genetic variation persists. Nevertheless, the current small population size is likely to lead to considerable inbreeding. Overall, our findings allow for optimism about the ongoing reintroduction of Raso larks to a nearby island, but also highlight the urgency of this effort.