Abstract The aye-aye (Daubentonia madagascariensis) is the only extant member of the Daubentoniidae primate family. Although several reference genomes exist for this endangered strepsirrhine primate, the predominant usage of short-read sequencing has resulted in limited assembly contiguity and completeness, and no protein-coding gene annotations have yet been released. Here, we present a novel, fully annotated, chromosome-level hybrid de novo assembly for the species based on a combination of Oxford Nanopore Technologies long reads and Illumina short reads and scaffolded using genome-wide chromatin interaction data—a community resource that will improve future conservation efforts as well as primate comparative analyses.
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Fossil lemurs from Egypt and Kenya suggest an African origin for Madagascar’s aye-aye
Abstract In 1967 G.G. Simpson described three partial mandibles from early Miocene deposits in Kenya that he interpreted as belonging to a new strepsirrhine primate,Propotto. This interpretation was quickly challenged, with the assertion thatPropottowas not a primate, but rather a pteropodid fruit bat. The latter interpretation has not been questioned for almost half a century. Here we re-evaluate the affinities ofPropotto, drawing upon diverse lines of evidence to establish that this strange mammal is a strepsirrhine primate as originally suggested by Simpson. Moreover, our phylogenetic analyses support the recognition ofPropotto, together with late EocenePlesiopithecusfrom Egypt, as African stem chiromyiform lemurs that are exclusively related to the extant aye-aye (Daubentonia) from Madagascar. Our results challenge the long-held view that all lemurs are descended from a single ancient colonization of Madagascar, and present an intriguing alternative scenario in which two lemur lineages dispersed from Africa to Madagascar independently, possibly during the later Cenozoic.
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- Award ID(s):
- 1638796
- PAR ID:
- 10153575
- Publisher / Repository:
- Nature Publishing Group
- Date Published:
- Journal Name:
- Nature Communications
- Volume:
- 9
- Issue:
- 1
- ISSN:
- 2041-1723
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Hurst, Laurence D (Ed.)Every mammal studied to date has been found to have a male mutation bias: male parents transmit more de novo mutations to offspring than female parents, contributing increasingly more mutations with age. Although male-biased mutation has been studied for more than 75 years, its causes are still debated. One obstacle to understanding this pattern is its near universality—without variation in mutation bias, it is difficult to find an underlying cause. Here, we present new data on multiple pedigrees from two primate species: aye-ayes (Daubentonia madagascariensis), a member of the strepsirrhine primates, and olive baboons (Papio anubis). In stark contrast to the pattern found across mammals, we find a much larger effect of maternal age than paternal age on mutation rates in the aye-aye. In addition, older aye-aye mothers transmit substantially more mutations than older fathers. We carry out both computational and experimental validation of our results, contrasting them with results from baboons and other primates using the same methodologies. Further, we analyze a set of DNA repair and replication genes to identify candidate mutations that may be responsible for the change in mutation bias observed in aye-ayes. Our results demonstrate that mutation bias is not an immutable trait, but rather one that can evolve between closely related species. Further work on aye-ayes (and possibly other lemuriform primates) should help to explain the molecular basis for sex-biased mutation.more » « less
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Abstract The nocturnal aye-aye, Daubentonia madagascariensis, is one of the most elusive lemurs on the island of Madagascar. The timing of its activity and arboreal lifestyle has generally made it difficult to obtain accurate assessments of population size using traditional census methods. Therefore, alternative estimates provided by population genetic inference are essential for yielding much needed information for conservation measures and for enabling ecological and evolutionary studies of this species. Here, we utilize genomic data from 17 individuals—including 5 newly sequenced, high-coverage genomes—to estimate this history. Essential to this estimation are recently published annotations of the aye-aye genome which allow for variation at putatively neutral genomic regions to be included in the estimation procedures, and regions subject to selective constraints, or in linkage to such sites, to be excluded owing to the biasing effects of selection on demographic inference. By comparing a variety of demographic estimation tools to develop a well-supported model of population history, we find strong support for two demes, separating northern Madagascar from the rest of the island. Additionally, we find that the aye-aye has experienced two severe reductions in population size. The first occurred rapidly, ∼3,000 to 5,000 years ago, and likely corresponded with the arrival of humans to Madagascar. The second occurred over the past few decades and is likely related to substantial habitat loss, suggesting that the species is still undergoing population decline and remains at great risk for extinction.more » « less
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Inferring fine-scale mutation and recombination rate maps in aye-ayes (Daubentonia madagascariensis)The rate of input of new genetic mutations, and the rate at which that variation is reshuffled, are key evolutionary processes shaping genomic diversity. Importantly, these rates vary not just across populations and species, but also across individual genomes. Despite previous studies having demonstrated that failing to account for rate heterogeneity across the genome can bias the inference of both selective and neutral population genetic processes, mutation and recombination rate maps have to date only been generated for a relatively small number of organisms. Here, we infer such fine-scale maps for the aye-aye (Daubentonia madagascariensis) – a highly endangered strepsirrhine that represents one of the earliest splits in the primate clade, and thus stands as an important outgroup to the more commonly-studied haplorrhines – utilizing a recently released fully-annotated genome combined with high-quality population sequencing data. We compare our indirectly inferred rates to previous pedigree-based estimates, finding further evidence of relatively low mutation and recombination rates in aye-ayes compared to other primates.more » « less
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Aye-ayes (Daubentonia madagascariensis) are one of the 25 most critically endangered primate species in the world. Endemic to Madagascar, their small and highly fragmented populations make them particularly vulnerable to both genetic disease and anthropogenic environmental changes. Over the past decade, conservation genomic efforts have largely focused on inferring and monitoring population structure based on single nucleotide variants to identify and protect critical areas of genetic diversity. However, the recent release of a highly contiguous genome assembly allows, for the first time, for the study of structural genomic variation (deletions, duplications, insertions, and inversions) which are likely to impact a substantial proportion of the species’ genome. Based on whole-genome, short-read sequencing data from 14 individuals, >1,000 high-confidence autosomal structural variants were detected, affecting ∼240 kb of the aye-aye genome. The majority of these variants (>85%) were deletions shorter than 200 bp, consistent with the notion that longer structural mutations are often associated with strongly deleterious fitness effects. For example, two deletions longer than 850 bp located within disease-linked genes were predicted to impose substantial fitness deficits owing to a resulting frameshift and gene fusion, respectively; whereas several other major effect variants outside of coding regions are likely to impact gene regulatory landscapes. Taken together, this first glimpse into the landscape of structural variation in aye-ayes will enable future opportunities to advance our understanding of the traits impacting the fitness of this endangered species, as well as allow for enhanced evolutionary comparisons across the full primate clade.more » « less
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