Sex chromosomes have evolved from the same autosomes multiple times across vertebrates, suggesting that selection for recombination suppression has acted repeatedly and independently on certain genetic backgrounds. Here, we perform comparative genomics of a bird clade (larks and their sister lineage; Alaudidae and Panuridae) where multiple autosome–sex chromosome fusions appear to have formed expanded sex chromosomes. We detected the largest known avian sex chromosome (195.3 Mbp) and show that it originates from fusions between parts of four avian chromosomes: Z, 3, 4A and 5. Within these four chromosomes, we found evidence of five evolutionary strata where recombination had been suppressed at different time points, and show that stratum age explained the divergence rate of Z–W gametologs. Next, we analysed chromosome content and found that chromosome 3 was significantly enriched for genes with predicted sex-related functions. Finally, we demonstrate extensive homology to sex chromosomes in other vertebrate lineages: chromosomes Z, 3, 4A and 5 have independently evolved into sex chromosomes in fish (Z), turtles (Z, 5), lizards (Z, 4A), mammals (Z, 4A) and frogs (Z, 3, 4A, 5). Our results provide insights into and support for repeated evolution of sex chromosomes in vertebrates.
Small effective population sizes could expose island species to inbreeding and loss of genetic variation. Here we investigate factors shaping genetic diversity in the Raso lark, which has been restricted to a single islet for ~500 years, with a population size of a few hundred. We assembled a reference genome for the related Eurasian skylark and then assessed diversity and demographic history using RAD-seq data (75 samples from Raso larks and two related mainland species). We first identify broad tracts of suppressed recombination in females, indicating enlarged neo-sex chromosomes. It is plausible that these regions might inadvertently and temporarily preserve pre-existing allelic variation in females that would otherwise be lost through genetic drift. We then show that genetic diversity across autosomes in the Raso lark is lower than in its mainland relatives, but inconsistent with long-term persistence at its current population size. Finally, we find that genetic signatures of the recent population contraction are overshadowed by an ancient expansion and persistence of a very large population until the human settlement of Cape Verde. Our findings show how genome-wide approaches to study endangered species can help avoid confounding effects of genome architecture on diversity estimates, and how present day diversity can be shaped by ancient demographic events.
Small effective population sizes could expose island species to inbreeding and loss of genetic variation. Here, we investigate factors shaping genetic diversity in the Raso lark, which has been restricted to a single islet for approximately 500 years, with a population size of a few hundred. We assembled a reference genome for the related Eurasian skylark and then assessed diversity and demographic history using RAD-seq data (75 samples from Raso larks and two related mainland species). We first identify broad tracts of suppressed recombination in females, indicating enlarged neo-sex chromosomes. We then show that genetic diversity across autosomes in the Raso lark is lower than in its mainland relatives, but inconsistent with long-term persistence at its current population size. Finally, we find that genetic signatures of the recent population contraction are overshadowed by an ancient expansion and persistence of a very large population until the human settlement of Cape Verde. Our findings show how genome-wide approaches to study endangered species can help avoid confounding effects of genome architecture on diversity estimates, and how present-day diversity can be shaped by ancient demographic events.
Evaluating the genetic and demographic independence of populations of threatened species is important for determining appropriate conservation measures, but different technologies can yield different conclusions. Despite multiple studies, the taxonomic status and extent of gene flow between the main breeding populations of Black-footed Albatross (Phoebastria nigripes), a Near-Threatened philopatric seabird, are still controversial. Here, we employ double digest RADseq to quantify the extent of genomewide divergence and gene flow in this species. Our genomewide data set of 9760 loci containing 3455 single nucleotide polymorphisms yielded estimates of genetic diversity and gene flow that were generally robust across seven different filtering and sampling protocols and suggest a low level of genomic variation (θ per site = ∼0.00002–0.00028), with estimates of effective population size (Ne = ∼500–15 881) falling far below current census size. Genetic differentiation was small but detectable between Japan and Hawaii (FST ≈ 0.038–0.049), with no FST outliers. Additionally, using museum specimens, we found that effect sizes of morphological differences by sex or population rarely exceeded 4%. These patterns suggest that the Hawaiian and Japanese populations exhibit small but significant differences and should be considered separate management units, although the evolutionary and adaptive consequences of this differentiation remain to be identified.
Islands have intrinsic geographic characteristics (isolation, small area) that contribute to exacerbated genetic threats to insular species. Isolation can make gene exchange difficult, which, coupled to the often small size of island populations, can increase these risks (Ferreira et al., 2016; Frankham, 1998). One striking example of the genetic threats to insular species is that of the last woolly mammoth Mammuthus primigenius population, where 300 individuals surviving on Wrangel Island are thought to have ultimately disappeared
Estimating and understanding variation in survival rates is crucial for the management of threatened species, especially those with limited population sizes and/or restricted ranges. Using a capture-resighting dataset covering 2004–2017, we estimate adult survival in the Raso lark Alauda razae, a Critically Endangered single-island Cape Verdean endemic, whose population varied 25-fold during the study. Average annual adult survival was similar for males (0.813 ± 0.011) and females (0.826 ± 0.011) over the period. These values are high for a temperate passerine but not unusual for an insular tropical species like the lark. The oldest bird was recorded 13 years after first ringing. There was strong evidence that survival varied among years (between 0.57 and 0.95), being generally higher in wetter years. Survival, especially of males, was lower when the population was large, but only in drier years. Survival declined with age but there was no evidence that this decline was other than linear. High survival, even in the face of dry conditions, at least when the population is depressed, has probably contributed to the persistence of the species on its 7 km2 island home over several centuries.
For species without parental care, such as sea turtles, nest site selection is particularly important for embryo development, hatchling survival and, ultimately, reproductive success. We conducted an 8-year (2012–2019) capture–mark–recapture study of the re-nesting behaviour of loggerhead turtles Caretta caretta to identify both inter- and intra-beach patterns of nest site selection. Our study site, Maio Island in the archipelago of Cabo Verde, hosts one of the largest loggerhead turtle nesting colonies globally. Of 1,060 females analysed, 77% laid repeated clutches within 15 km of their previous nesting sites both between and within nesting seasons. This site fidelity was particularly high (64–71%) for turtles nesting on the east coast of Maio Island. In two areas of the island (north-west and south-east) individual nesting zone consistency was extremely low (10–25%). In all cases extra-zone re-nesting events mainly occurred on the east coast. We also found that females avoided re-nesting near the shoreline, which is particularly relevant in the context of rising sea levels. Overall, loggerhead turtles nesting in Maio Island are philopatric but are using a bet-edging strategy to distribute nests amongst several beaches, choosing the safest area within each beach to maximize their reproductive success. This study highlights the priority sites for protection on Maio Island and could help to optimize capture–mark–recapture programmes. The data reveal the potential for adaptive responses to projected sea level rises.
Sex chromosomes have evolved from the same autosomes multiple times across vertebrates, suggesting that certain genomic regions are predisposed towards sex-linkage. However, to test this hypothesis detailed studies of independently originated sex-linked regions and their gene content are needed. Here we address this problem through comparative genomics of birds where multiple chromosomes appear to have formed neo-sex chromosomes: larks (Alaudidae; Sylvioidea). We detected the largest known avian sex chromosome (195.3 Mbp) and show that it originates from fusions between (parts of) four avian chromosomes (Z, 3, 4A and 5). We found evidence of five evolutionary strata where recombination has been suppressed at different time points, and that these time points correlate with the level of Z–W gametolog differentiation. We show that there is extensive homology to sex chromosomes in other vertebrate lineages: three of the fused chromosomes (Z, 4A, 5) have independently evolved into sex chromosomes in fish (Z), turtles (Z, 5), lizards (Z, 4A) and mammals (Z, 4A). Moreover, we found that the fourth chromosome, chromosome 3, was significantly enriched for genes with predicted sex-specific functions. These results support a key role of chromosome content in the evolution of sex chromosomes in vertebrates.
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