Evolutionary history inferred from the de novo assembly of a nonmodel organism, the blue‐eyed black lemur

Abstract

Lemurs, the living primates most distantly related to humans, demonstrate incredible diversity in behaviour, life history patterns and adaptive traits. Although many lemur species are endangered within their native Madagascar, there is no high-quality genome assembly from this taxon, limiting population and conservation genetic studies. One critically endangered lemur is the blue-eyed black lemur Eulemur flavifrons. This species is fixed for blue irises, a convergent trait that evolved at least four times in primates and was subject to positive selection in humans, where 5′ regulatory variation of OCA2 explains most of the brown/blue eye colour differences. We built a de novo genome assembly for E. flavifrons, providing the most complete lemur genome to date, and a high confidence consensus sequence for close sister species E. macaco, the (brown-eyed) black lemur. From diversity and divergence patterns across the genomes, we estimated a recent split time of the two species (160 Kya) and temporal fluctuations in effective population sizes that accord with known environmental changes. By looking for regions of unusually low diversity, we identified potential signals of directional selection in E. flavifrons at MITF, a melanocyte development gene that regulates OCA2 and has previously been associated with variation in human iris colour, as well as at several other genes involved in melanin biosynthesis in mammals. Our study thus illustrates how whole-genome sequencing of a few individuals can illuminate the demographic and selection history of nonmodel species.

Application of PE‐RADSeq to the study of genomic diversity and divergence of two Brazilian marmoset species (Callithrix jacchusandC. penicillata)

“…If indeed there was a strong bias in favor of C. jacchus mapping to the Callithrix reference genome over C. penicillata, we would expect Overall, our results were close to the C. jacchus nucleotide levels (π = 0.00123) reported by Leffler et al (2012). C. jacchus and C. penicillata show higher nucleotide diversity than Homo sapiens (π = 0.0007-0.0012), but marmosets and humans are on the lower end of the scale of nucleotide diversity values in primates (Leffler et al, 2012;Meyer et al, 2015). Leffler et al (2012) pointed out that the evolutionary forces that maintain genetic diversity in species are still not well understood but genomic surveys of diversity, like those we report here for Callithrix, are an important first step to resolving this question.…”

Climate change and human colonization triggered habitat loss and fragmentation in Madagascar

“…With the exception of Olivieri, Sousa, Chikhi, and Radespiel (), who studied the demographic history of three mouse lemur species, previous demographic inferences in lemurs and other Malagasy species investigated only a single species and a restricted number of sampling locations (Lawler, , ; Louis et al., ; Markolf, Roos, & Kappeler, ). Moreover, in most cases, population structure is ignored (Lawler, ; Markolf et al., ; Meyer et al., ) and even when it is accounted for, only a single inferential approach was used (Quéméré et al., ). Here, we used several methods and considered population structure and population size changes together in a combined framework.…”

“…The increasing availability of genomic data (including lemurs: mouse lemur, aye‐aye and eulemur—Perry et al., , ; Meyer et al., ; P. coquereli’ s—GCA_000956105.1; and P. tattersalli —SRX701290‐93) coupled with the recent development of methods to infer demographic history from genomic data (Li & Durbin, ; Liu & Fu, ; Mazet et al., ; Salmona, Heller, Lascoux & Shafer, ) promise to resolve demographic history of species with unprecedented resolution. Although their application is challenging for noninvasive DNA (that include exogenous plant, fungi and bacteria DNA; Lynn, Sechi, Chikhi, & Goossens, ), capture approaches (e.g., Fabbri et al., ; Perry, Marioni, Melsted, & Gilad, ) associated with reduction in genome complexity (e.g., RAD; Suchan et al., ; Ali et al., ; Hoffberg et al., ) promise to alleviate these challenges.…”

Conservation genomic analysis reveals ancient introgression and declining levels of genetic diversity in Madagascar’s hibernating dwarf lemurs

“…Admixture between Neanderthals and modern humans has, for example, left detectable signatures in the genome sequences of modern humans (Harris and Nielsen 2016), which can be identified in the genome sequences of single individuals (Green et al 2010a;Hajdinjak et al 2018;Slon et al 2018). A focus on making use of the entirety of information contained within a single genome has also been beneficial for a number of non-human study systems where the ability to collect and sequence many samples is prohibitively difficult (Prado-martinez et al 2013;Meyer et al 2015;Palkopoulou et al 2015;Abascal et al 2016;Figueiró et al 2017;Rogers and Slatkin 2017;Árnason et al 2018).…”