Biology subjects

Yoder, A. D.

Publications and source records attributed to Yoder, A. D..

At least 19 recordsLinked to original sources

bioRxiv2026

Predation of small nocturnal primates (Microcebus) on Madagascar; insights into predator preferences in Andohahela National Park

Predation is a major selective force shaping lemur behaviour and population dynamics, yet direct observations remain rare, particularly for small nocturnal species. Here, we document predation on mouse lemurs (Microcebus spp., Cheirogaleidae) in Andohahela National Park, south-eastern Madagascar, and using complementary evidence from radio-telemetry and owl pellet analyses. Two radio-collared individuals were confirmed as prey of endemic snakes, Ithycyphus oursi and Madagascarophis meridionalis (both Pseudoxyrhophiidae), representing the first documented records of Microcebus predation by these species. Examination of owl pellets and prey remains from three sites and from three owl species revealed a single predation event by Asio madagascariensis (Strigidae), likely involving M. tanosi, no evidence of mouse lemur predation by Tyto alba (Tytonidae) despite high local prey availability, and a single and first predation record from Athene superciliaris (Strigidae). Material from A. superciliaris roosts was otherwise dominated by invertebrates, indicating that primate predation is likely opportunistic. Together, these findings expand the known predator guild of mouse lemurs and suggest that snake predation is rarely detected, and its contribution to mouse lemur mortality and population dynamics is likely underestimated. Our findings demonstrate how combining behavioural field observations with dietary evidence can uncover otherwise undetected predation events and clarify predator prey relationships in nocturnal primates.

ecology↗

bioRxiv2026

Diet and feeding strategies of two sympatric mouse lemurs (Microcebus) in the xeric forests of Andohahela, southeastern Madagascar

Understanding how closely related species coexist in highly seasonal and unpredictable environments is central to studies of ecological differentiation and niche partitioning. We investigated the feeding ecology of sympatric populations of Microcebus murinus and M. griseorufus within a contact zone in Andohahela National Park, southeastern Madagascar, across dry and wet seasons. Using a combination of direct behavioral observations (1,611 feeding records), fecal sample analyses (n = 56), and vegetation phenology surveys, we quantified dietary composition, seasonal shifts in resource use, and habitat-related variation. Seasonal changes in diet were pronounced, with dry-season feeding dominated by exudates and wet-season diets incorporating greater proportions of fruit and flowers, closely tracking phenological patterns at both sites. Diets of both species were dominated by plant resources, but consistent interspecific differences in dietary strategy were evident. Although both species consumed comparable proportions of insect prey, M. murinus showed pronounced wet-season increases in the use of high-sugar, carbohydrate-rich floral resources (15.9%) and hemipteran-associated honeydew (30.6%). In contrast, M. griseorufus relied more consistently on predictable exudates throughout the year. Fecal analyses supported observational data but revealed differences in the detectability of dietary components, with increased representation of invertebrates in the wet season and seeds in the dry season. These results indicate substantial dietary overlap but consistent differences in resource use, suggesting that coexistence is facilitated by fine-scale trophic differentiation within a broadly shared omnivorous niche. Such subtle but persistent differences in feeding strategy likely reduce competitive overlap and enable continued sympatry in a climatically variable and resource-limited system.

ecology↗

bioRxiv2026

Rapid centromere turnover and the adaptive radiation of lemurs

Centromeres represent essential chromosomal structures required for faithful chromosome segregation during cell division but are paradoxically hypermutable, leading to centromere drive and reproductive isolation in closely related species. Using long-read sequencing, we generate nearly complete genomes (2.1-2.5 Gbp) from eight lemur species and characterize the sequence, epigenetic and cytogenetic structure of 223 strepsirrhini centromeres providing an alternative primate perspective of centromere evolution. No lemur centromere consists of -satellite DNA that typifies the haplorhine lineage; instead, each species evolved its own distinct higher-order centromeric repeat sequence, varying substantially in both monomer length (ranging from 41-548 bp) and primary sequence composition (GC percentages 28.7-67.9%) including centromere cooption of telomeric repeats in brown lemurs. Most centromeres show characteristic hypomethylation dip regions (110-300 kbp) as candidates for kinetochore attachment. The centromere sequence motif shows no apparent sequence homology among lemur genera, even for species separated by less than 15 million years (Lemur and Eulemur). We estimate a >6-fold increased rate in primary centromeric motif turnover in strepsirrhines when compared to haplorhines and this occurred in conjunction with positive selection of the CENP-B protein in lemur lineages. We propose that lemur radiation and centromere diversification are linked, whereby accelerated motif turnover provides a stasipatric barrier contributing to rapid chromosomal evolution.

genomics↗

bioRxiv2024

Unprecedented female mutation bias in aye-ayes

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 madagascarensis), 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.

evolutionary biology↗

bioRxiv2023

Not one, but multiple radiations underlie the biodiversity of Madagascar's endangered lemurs

Lemurs are often cited as an example of adaptive radiation. Since colonizing Madagascar, more than 100 extant lemur species have evolved to fill a variety of ecological niches on the island. However, recent work suggests that lemurs do not exhibit one of the hallmarks of other adaptive radiations: explosive speciation rates that decline over time. Thus, characterizing the tempo and mode of evolution in lemurs can help us understand alternative ways that hyperdiverse clades arise over time, which might differ from traditional models. We explore the evolution of lemurs using a phylogenomic dataset with broad taxonomic sampling that includes the lemurs sister group, the lorisiforms of Asia and continental Africa. Our analyses reveal multiple bursts of diversification (without subsequent declines) that explain much of todays lemur diversity. We also find higher rates of speciation in Madagascars lemurs compared to lorisiforms, and we demonstrate that the lemur clades with exceptionally high diversification rates have higher rates of genomic introgression. This suggests that hybridization in these primates is not an evolutionary dead-end, but a driving force for diversification. Considering the conservation crisis affecting strepsirrhine primates, with approximately 95% of species being threatened with extinction, this phylogenomic study offers a new perspective for explaining Madagascars exceptional primate diversity and reveals patterns of speciation, extinction, and gene flow that will help inform future conservation decisions.

evolutionary biology↗

bioRxiv2023

Genetic variation in Loudetia simplex supports the presence of ancient grasslands in Madagascar

O_LIResearch Aims -- The extent of Madagascars grasslands prior to human colonization is unresolved. We used population genetic analyses of a broadly dominant C4 fire-adapted grass, Loudetia simplex, as a proxy for estimating grassland change through time. We carefully examined the utility of target-enrichment data for population genetics to make recommendations for conservation genetics. We explored the potential of estimating individual ploidy levels from target-enrichment data and how assumptions about ploidy could affect analyses. C_LIO_LIMethods -- We developed a novel bioinformatic pipeline to estimate ploidy and genotypes from target-enrichment data. We estimated standard population genetic summary statistics in addition to species trees and population structure. Extended Bayesian skyline plots provided estimates of population size through time for empirical and simulated data. C_LIO_LIKey Result -- All Malagasy Loudetia simplex individuals sampled in this study formed a clade and possibly indicated an ancestral Central Highland distribution of 800m in altitude and above. Demographic models suggested grassland expansions occurred prior to the Last Interglacial Period and supported extensive grasslands prior to human colonization. Though there are limitations to target-enrichment data for population genetic studies, we find that analyses of population structure are reliable. C_LIO_LIKey Point --Genetic variation in Loudetia simplex supports widespread grasslands in Madagascar prior to the more recent periods of notable paleoclimatic change. However, the methods explored here could not differentiate between paleoclimatic change near the Last Glacial Maximum and anthropogenic effects. Target-enrichment data can be a valuable tool for analyses of population structure in the absence a reference genome. C_LI Societal Impact StatementRecognizing Loudetia dominated grasslands were widespread prior to human colonization highlights that open ecosystems were and continue to be an important component of Madagascars biodiversity. Urgently required are biodiversity inventories and integrative taxonomic treatments of grassland flora and fauna to asses risks to understudied ecosystems historically regarded as wastelands. Substantial financial and logistical barriers exist to implementing conservation studies using contemporary genomic tools. We ameliorated some of the challenges for population genetic analyses of non-model polyploids lacking reference genomes by developing computational resources to leverage a cost-effective data generation strategy that requires no prior genetic knowledge of the target species. ResumeO_LILes objectifs de la recherche -- Letendue des ecosystemes ouverts de Madagascar avant la colonisation humaine reste a eclaircir. Nous avons utilise une analyse de la population genetique dune graminee C4 adaptee au feu, largement dominante, Loudetia simplex, comme reference pour estimer les changements au niveau de ces biomes au fil du temps. Nous avons examine attentivement lutilite des donnees denrichissement cible pour la genetique de population afin de formuler des recommandations pour la conservation genetique. Nous avons explore le potentiel de lestimation du niveau des ploidies individuelles a partir des donnees denrichissement cible et comment les hypotheses a propos de ces ploidies pourraient affecter les analyses. C_LIO_LILes methodes -- Nous avons developpe un nouveau canal bioinformatique pour estimer les ploidies et les genotypes a partir des donnees denrichissement cible. Nous avons estime les statistiques standard de la population genetique, en plus des arbres des especes et de la structure de la population. Lutilisation des traces etendus du ciel bayesien a fourni une estimation de la taille de la population au fil du temps pour des donnees empiriques et simulees. C_LIO_LIResultat cle -- Tous les individus Malagasy de Loudetia simplex echantillonnes dans cette etude ont forme un clade, indiquant une eventuelle ancienne distribution dans les hauts plateaux. Les modeles demographiques suggerent une expansion des prairies bien avant la derniere periode interglaciaire et soutiennent lexistence dune vaste distribution avant la colonisation humaine. Bien quil y ait des limites a lenrichissement des donnees cibles pour letude de la genetique des populations, nous constatons que lanalyse des structures des populations est fiable. C_LIO_LILes points cles -- La variation genetique de Loudetia simplex soutient lexistence de vastes prairies a Madagascar avant les periodes plus recentes de changements paleoclimatiques notables. Cependant, les methodes explorees ici nont pas permis de faire la difference entre les changements paleoclimatiques pres du dernier maximum glaciaire et les effets anthropogenes. Les donnees denrichissement cible peuvent etre un outil precieux pour les analyses de la structure des populations en labsence dun genome de reference. C_LI Declaration dimpact societalReconnaitre que les prairies dominees par Loudetia etaient repandues avant la colonisation humaine souligne que les ecosystemes ouverts etaient et continuent detre un composant important de la biodiversite de Madagascar. Il est urgent de realiser des inventaires de la biodiversite et une taxonomie integree pour le traitement de la flore et de la faune des ecosystemes ouverts afin devaluer les risques pour les ecosystemes sous-etudies consideres historiquement comme des terres en friches. Des barrieres financieres et logistiques existent pour mettre en uvre letude de la conservation en utilisant les outils genomiques contemporains. Nous avons ameliore certains des defis lies aux analyses genetiques de populations de polyploides non modeles, sans genomes de reference, en developpant des ressources informatiques pour exploiter une strategie pouvant generer des donnees rentables ne necessitant aucune connaissance genetique prealable de lespece cible. FamintinanaO_LINy tanjonny fikarohana -- Mbola tsy fantatra mazava tsara ny fivelaranny hivoka teto Madagasikara talohanny fahatongavany olombelona. Mba ahafantarana ny fihovana nitranga nandritra ny fotoana naharitra teo aminireo hivoka ireo dia nanao famakafakahana ara-genetika aminny ahitra C4 miompana aminny afo iray antsoina Loudetia simplex ara-tsiantifika na Berambo na Hara aminny teny malagasy izahay. Nandinika tsara ny maha-zava-dehibe ny fampitomboana ny antotan-kevitra mba ahafahana manolo-kevitra momba ny fiarovana ny fototarazo genetika. Nandinika ny mety mampiavaka ny fanombanana anny ploidy tsirairay aminny fampitomboana antotan-kevitra sy ny mety ho fiantraikanny fiheverana momba ireo ploidy ireo aminny fikarohana. C_LIO_LIFomba Fiasa -- Namorona fantsona bioinformatika vaovao mba ahafahana manombana ny ploidy sy ny << genotypes >> avy aminny antotan-kevitra nokendrena izahay. Notombanana ny antontanisa famintinana ny fototarazo ara-genetikanireo vondronahitra ireo, miampy ny karazana hazo sy ny firafitry ny vondrona na koa hoe mponina. Nanome tombantombana ny habenny mponina aminny alalanny fotoana ny antontan-kevitra voavinavina azo taminny fikarohana. Fikarohana izay azo taminny alalanny << Bayesina Skuline Plots >>. C_LIO_LIVokam-pikarohana fototra -- Ny vondrona Loudetia simplex eto Madagasikara izay niasana dia namorona << clade >> na fikambanana iray, izay manondro ny mety maha ela netezana sy tranainy anio ahitra io eny aminny faritra avo. Ny modely demografika dia manoro hevitra aminny naha be velarana ny hivoka izay efa ela talohanny vanim-potoana << interglacial >> farany ary manohana ny fivelarana midadasika anireo kijana ireo alohanny fonenanny olombelona. Na dia misy fetrany aza ny fampitomboana ny antotan-kevitra kendrena aminny fandalinana ny fototarazo genetika mombanny mponina, dia hita fa azo itokisana ny fikarohana natao mombanny firafitry ny mponina. C_LIO_LIHevi-dehibe -- Ny fahasamihafana ara-genetika ao aminny Loudetia simplex dia manohana ny fisianny hivoka na kijana midadasika eto Madagasikara talohanny vanim-potoananny fiovana paleoclimatika nisongadina. Na izany aza, ny fombam-pikarohana nampiasana teto dia tsy nahavita nanavaka ny fiovanny paleoclimatika akaikinny vanim-potoana lehibe nangatsiaka farany sy ny vokatry ny fitrandrahana nataonny olombelona. Mety ho fitaovana manan-danja aminny famakafakana ny firafitry ny mponina ny antotan-kevitra nampitombona na dia tsy misy fitaovana genomika iangaina aza. C_LI Fanambarana fiantraika ara-tsosialyNy fanekena fa niely patrana ny hivoka itoeranny Loudetia talohanny fanjanahanny olombelona dia manamarika fa ireo hivoka ireo dia singa manan-danja aminny zavamananaina eto Madagasikara. Ilaina maika ny fahafantarana ara biolojika sy taxononomique ny zavamaniry sy ny biby aminny hivoka mba hanombanana ny loza mety hitranga aminny hivoka izay tsy ananana fahalalana maro sady heverina ho tany maina. Misy sakana ara-bola sy ara-pitaovana aminny fampiharana ny fandalinana momba ny fiarovana izay nampiasana fitaovana genomika ankehitriny. Nohatsarainay ny sasany aminireo fanamby mifandraika aminny famakafakana ara-genetika ny mponina manana ploidy maro tsy modely, izay tsy misy fitaovana genomika iaingana, aminny alalanny fampivoarana loharanon-kevitra kajy mba hitrandrahana paikady izay mety hiteraka angon-drakitra mahomby tsy mitaky fahalalana mahakasika ny fototarazo ara-genetika ny zava-maniry izay tiana karohina.

evolutionary biology↗

bioRxiv2021

Mutationathon: towards standardization in estimates of pedigree-based germline mutation rates

In the past decade, several studies have estimated the human per-generation germline mutation rate using large pedigrees. More recently, estimates for various non-human species have been published. However, methodological differences among studies in detecting germline mutations and estimating mutation rates make direct comparisons difficult. Here, we describe the many different steps involved in estimating pedigree-based mutation rates, including sampling, sequencing, mapping, variant calling, filtering, and how to appropriately account for false-positive and false-negative rates. For each step, we review the different methods and parameter choices that have been used in the recent literature. Additionally, we present the results from a "Mutationathon", a competition organized among five research labs to compare germline mutation rate estimates for a single pedigree of rhesus macaques. We report almost a two-fold variation in the final estimated rate among groups using different post-alignment processing, calling, and filtering criteria and provide details into the sources of variation across studies. Though the difference among estimates is not statistically significant, this discrepancy emphasizes the need for standardized methods in mutation rate estimations and the difficulty in comparing rates from different studies. Finally, this work aims to provide guidelines for computational and statistical benchmarks for future studies interested in identifying germline mutations from pedigrees.

evolutionary biology↗

bioRxiv2021

RADseq data reveal a lack of admixture in a mouse lemur contact zone contrary to previous microsatellite results

Despite being one of the most fundamental biological processes, the process of speciation remains poorly understood in many groups of organisms. Mouse lemurs are a species-rich genus of small primates endemic to Madagascar, whose diversity has only recently been uncovered using genetic data and is primarily found among morphologically cryptic, allopatric populations. To assess to what extent described species represent reproductively isolated entities, studies are needed in areas where mouse lemur taxa come into contact. Hybridization has previously been reported in a contact zone between two closely related mouse lemur species (Microcebus murinus and M. griseorufus) based on microsatellite data. Here, we revisit this system using RADseq data for populations in, near, and far from the contact zone, including many of the individuals that had previously been identified as hybrids. Surprisingly, we find no evidence for admixed nuclear ancestry in any of the individuals. Re-analyses of microsatellite data and simulations suggest that previously inferred hybrids were false positives and that the program NewHybrids can be particularly sensitive to erroneously inferring hybrid ancestry. Using coalescent-bases analyses, we also show an overall lack of recent gene flow between the two species, and low levels of ancestral gene flow. Combined with evidence for local syntopic occurrence, these data indicate that M. murinus and M. griseorufus are reproductively isolated. Finally, we estimate that they diverged less than a million years ago, suggesting that completion of speciation is relatively rapid in mouse lemurs. Future work should focus on the underpinnings of reproductive isolation in this cryptic primate radiation, which are mostly unknown. Our study also provides a cautionary tale for the inference of hybridization with microsatellite data.

evolutionary biology↗

bioRxiv2021

Molecular adaptation to folivory and the conservation implications for Madagascar's lemurs

Folivory evolved independently at least three times over the last 40 million years among Madagascars lemurs. Many extant lemuriform folivores exist in sympatry in Madagascars remaining forests. These species avoid feeding competition by adopting different dietary strategies within folivory, reflected in behavioral, morphological, and microbiota diversity across species. These conditions make lemurs an ideal study system for understanding adaptation to leaf-eating. Most folivorous lemurs are also highly endangered. The significance of folivory for conservation outlook is complex. Though generalist folivores may be relatively well equipped to survive habitat disturbance, specialist folivores occupying narrow dietary niches may be less resilient. Characterizing the genetic bases of adaptation to folivory across species and lineages can provide insights into their differential physiology and potential to resist habitat change. We recently reported accelerated genetic change in RNASE1, a gene encoding an enzyme (RNase 1) involved in molecular adaptation in mammalian folivores, including various monkeys and sifakas (genus Propithecus; family Indriidae). Here, we sought to assess whether other lemurs, including phylogenetically and ecologically diverse folivores, might show parallel adaptive change in RNASE1 that could underlie a capacity for efficient folivory. We characterized RNASE1 in 21 lemur species representing all five families and members of the three extant folivorous lineages: 1) bamboo lemurs (family Lemuridae), 2) sportive lemurs (family Lepilemuridae), and 3) indriids (family Indriidae). We found pervasive sequence change in RNASE1 across all indriids, a dN/dS value > 3 in this clade, and evidence for shared change in isoelectric point, indicating altered enzymatic function. Sportive and bamboo lemurs, in contrast, showed more modest sequence change. The greater change in indriids may reflect a shared strategy emphasizing complex gut morphology and microbiota to facilitate folivory. This case study illustrates how genetic analysis may reveal differences in functional traits that could influence species ecology and, in turn, their resilience to habitat change. Moreover, our results support the contention that not all primate folivores are built the same and highlight the need to avoid generalizations about dietary guild in considering conservation outlook, particularly in lemurs where such diversity in folivory has probably led to extensive specialization via niche partitioning.

ecology↗

bioRxiv2021

Phasing Alleles Improves Network Inference with Allopolyploids

Accurately reconstructing the reticulate histories of polyploids remains a central challenge for understanding plant evolution. Although phylogenetic networks can provide insights into relationships among polyploid lineages, inferring networks may be hindered by the complexities of homology determination in polyploid taxa. We use simulations to show that phasing alleles from allopolyploid individuals can improve phylogenetic network inference under the multispecies coalescent by obtaining the true network with fewer loci compared to haplotype consensus sequences or sequences with heterozygous bases represented as ambiguity codes. Phased allelic data can also improve divergence time estimates for networks, which is helpful for evaluating allopolyploid speciation hypotheses and proposing mechanisms of speciation. To achieve these outcomes in empirical data, we present a novel pipeline that leverages a recently developed phasing algorithm to reliably phase alleles from polyploids. This pipeline is especially appropriate for target enrichment data, where depth of coverage is typically high enough to phase entire loci. We provide an empirical example in the North American Dryopteris fern complex that demonstrates insights from phased data as well as the challenges of network inference. We establish that our pipeline (PATE: Phased Alleles from Target Enrichment data) is capable of recovering a high proportion of phased loci from both diploids and polyploids. These data may improve network estimates compared to using haplotype consensus assemblies by accurately inferring the direction of gene flow, but statistical non-identifiability of phylogenetic networks poses a barrier to inferring the evolutionary history of reticulate complexes.

evolutionary biology↗

bioRxiv2020

Evolutionary and phylogenetic insights from a nuclear genome sequence of the extinct, giant subfossil koala lemur Megaladapis edwardsi

No endemic Madagascar animal with body mass >10 kg survived a relatively recent wave of extinction on the island. From morphological and isotopic analyses of skeletal subfossil remains we can reconstruct some of the biology and behavioral ecology of giant lemurs (primates; up to ~160 kg), elephant birds (up to ~860 kg), and other extraordinary Malagasy megafauna that survived well into the past millennium. Yet much about the evolutionary biology of these now extinct species remains unknown, along with persistent phylogenetic uncertainty in some cases. Thankfully, despite the challenges of DNA preservation in tropical and sub-tropical environments, technical advances have enabled the recovery of ancient DNA from some Malagasy subfossil specimens. Here we present a nuclear genome sequence (~2X coverage) for one of the largest extinct lemurs, the koala lemur Megaladapis edwardsi (~85kg). To support the testing of key phylogenetic and evolutionary hypotheses we also generated new high-coverage complete nuclear genomes for two extant lemur species, Eulemur rufifrons and Lepilemur mustelinus, and we aligned these sequences with previously published genomes for three other extant lemur species and 47 non-lemur vertebrates. Our phylogenetic results confirm that Megaladapis is most closely related to the extant Lemuridae (typified in our analysis by E. rufifrons) to the exclusion of L. mustelinus, which contradicts morphology-based phylogenies. Our evolutionary analyses identified significant convergent evolution between M. edwardsi and extant folivorous primates (colobine monkeys) and ungulate herbivores (horses) in genes encoding protein products that function in the biodegradation of plant toxins and nutrient absorption. These results suggest that koala lemurs were highly adapted to a leaf-based diet, which may also explain their convergent craniodental morphology with the small-bodied folivore Lepilemur.

genomics↗

bioRxiv2020

Comparative analyses of two primate species diverged by more than 60 million years show different rates but similar distribution of genome-wide UV repair events

Nucleotide excision repair is the primary DNA repair mechanism that removes bulky DNA adducts such as UV-induced pyrimidine dimers. Correspondingly, genome-wide mapping of nucleotide excision repair with eXcision Repair sequencing (XR-seq), provides comprehensive profiling of DNA damage repair. A number of XR-seq experiments at a variety of conditions for different damage types revealed heterogenous repair in the human genome. Although human repair profiles were extensively studied, how repair maps vary between primates is yet to be investigated. Here, we characterized the genome-wide UV-induced damage repair in gray mouse lemur, Microcebus murinus, in comparison to human. Mouse lemurs are strictly nocturnal, are the worlds smallest living primates, and last shared a common ancestor with humans at least 60 million years ago. We derived fibroblast cell lines from mouse lemur, exposed them to UV irradiation. The following repair events were captured genome-wide through the XR-seq protocol. Mouse lemur repair profiles were analyzed in comparison to the equivalent human fibroblast datasets. We found that overall UV sensitivity, repair efficiency, and transcription-coupled repair levels differ between the two primates. Despite this, comparative analysis of human and mouse lemur fibroblasts revealed that genome-wide repair profiles of the homologous regions are highly correlated. This correlation is stronger for the highly expressed genes. With the inclusion of an additional XR-seq sample derived from another human cell line in the analysis, we found that fibroblasts of the two primates repair UV-induced DNA lesions in a more similar pattern than two distinct human cell lines do. Our results suggest that mouse lemurs and humans, and possibly primates in general, share a homologous repair mechanism as well as genomic variance distribution, albeit with their variable repair efficiency. This result also emphasizes the deep homologies of individual tissue types across the eukaryotic phylogeny.

genomics↗

bioRxiv2020

Phylogeographic analysis of Goodman's mouse lemur reveals historical interconnectivity of Madagascar's Central Highlands and eastern rainforests

The Central Highland Plateau of Madagascar is largely composed of grassland savanna, interspersed with patches of closed-canopy forest. Conventional wisdom has it that these grasslands are anthropogenic in nature, having been created very recently via human agricultural practices. Yet, the ancient origins of the endemic grasses suggest that the extensive savannas are natural biomes, similar to others found around the globe. We use a phylogeographic approach to compare these two competing scenarios. By sampling multiple populations of Goodmans mouse lemur (Microcebus lehilahytsara), a small-bodied nocturnal primate, we reconstruct the phylogeographic and demographic history of these "environmental metronomes" to estimate the time at which their populations diverged, and thus proximally, when their habitats would have become fragmented. We applied coalescent methods to RADseq data to infer phylogenetic relationships, population structure, and migration corridors among sampling sites. These analyses indicate that forest fragmentation occurred rapidly during a period of decreased precipitation near the last glacial maximum and would have affected both the Central Highlands and eastern forests. Though there is clear genomic structure separating the populations of the Central Highland from those of the eastern rainforests, there is also evidence of historical migration between them. Findings support the hypothesis that the Central Highland savanna predates human arrival, indicating that it is a natural landscape that has long impacted the population dynamics of Goodmans mouse lemur, and by extension, other forest-dwelling organisms in Madagascar.

evolutionary biology↗

bioRxiv2019

Complex processes of cryptic speciation in mouse lemurs from a micro-endemism hotspot in Madagascar

AO_SCPLOWBSTRACTC_SCPLOWMouse lemurs (Microcebus) are a radiation of morphologically cryptic primates distributed throughout Madagascar for which the number of recognized species has exploded in the past two decades. This taxonomic explosion has prompted understandable concern that there has been substantial oversplitting in the mouse lemur clade. Here, we take an integrative approach to investigate species diversity in two pairs of sister lineages that occur in a region in northeastern Madagascar with high levels of microendemism and predicted habitat loss. We analyzed RADseq data with multispecies coalescent (MSC) species delimitation methods for three named species and an undescribed lineage previously identified to have divergent mtDNA. Marked differences in effective population sizes, levels of gene flow, patterns of isolation-by-distance, and species delimitation results were found among them. Whereas all tests support the recognition of the presently undescribed lineage as a separate species, the species-level distinction of two previously described species, M. mittermeieri and M. lehilahytsara is not supported - a result that is particularly striking when using the genealogical discordance index (gdi). Non-sister lineages occur sympatrically in two of the localities sampled for this study, despite an estimated divergence time of less than 1 Ma. This suggests rapid evolution of reproductive isolation in the focal lineages, and in the mouse lemur clade generally. The divergence time estimates reported here are based on the MSC and calibrated with pedigree-based mutation rates and are considerably more recent than previously published fossil-calibrated concatenated likelihood estimates, however. We discuss the possible explanations for this discrepancy, noting that there are theoretical justifications for preferring the MSC estimates in this case.

evolutionary biology↗

bioRxiv2019

Pedigree-based measurement of the de novo mutation rate in the gray mouse lemur reveals a high mutation rate, few mutations in CpG sites, and a weak sex bias

Spontaneous germline mutations are the raw material on which evolution acts, and knowledge of their frequency and genomic distribution is crucial for understanding how evolution operates at both long and short timescales. At present, the rate and spectrum of de novo mutations have been directly characterized in only a few lineages. It is therefore critical to expand the phylogenetic scope of these studies to gain a more general understanding of observed mutation rate patterns. Our study provides the first direct mutation rate estimate for a strepsirrhine (i.e., the lemurs and lorises), which comprise nearly half of the primate clade. Using high-coverage linked-read sequencing for a focal quartet of gray mouse lemurs (Microcebus murinus), we estimated the mutation rate to be 1.64 x 10-8 (95% credible interval: 1.41 x 10-8 to 1.98 x 10-8) mutations/site/generation. This estimate is higher than those measured for most previously characterized mammals. Further, we found an unexpectedly low count of paternal mutations, and only a modest overrepresentation of mutations at CpG-sites. Given the surprising nature of these observations, we conducted an independent analysis of context-dependent substitution types for gray mouse lemur and five additional primate species. This analysis yielded patterns consistent with the mutation spectrum from the pedigree mutation-rate analysis, which provides confidence in our ability to accurately identify de novo mutations with our data and bioinformatic filters.

evolutionary biology↗

bioRxiv2019

Next-generation in situ conservation and capacity building in Madagascar using a mobile genetics lab

Madagascar is a biodiversity hotspot that is facing rapid rates of deforestation, habitat destruction and poverty. Urgent action is required to document the status of biodiversity to facilitate efficacious conservation plans. Within country, new generations of Malagasy scientists and conservationists are taking on leadership roles, although many lack access to modern genetic sequencing and are underrepresented in academic publications, when compared to international counterparts.\n\nWith the recent advent of portable and affordable genetic technologies, it is now possible to tackle logistical considerations. Mobile genetics labs, with the capacity for in situ DNA extraction, amplification and sequencing, can produce scientifically reproducible data under field conditions, minimizing the time between sample collection and data analysis. Additionally, mobile labs offer powerful training opportunities for in-country scientists that enable local students and researchers to actively participate and contribute fully to the research enterprise, and that further empower these communities to contribute to the conservation dialog.\n\nHere, we show \"proof of concept\" by deploying a miniaturized thermal cycler alongside the Oxford Nanopore MinION DNA sequencer in Madagascar, including in the newly established Anjajavy Protected Area in northwestern Madagascar. We successfully extracted DNA from tissue samples collected using minimally-invasive techniques, amplified and sequenced a phylogenetically informative mitochondrial gene (cytochrome-b; cytb), and thereby confirmed the presence of Danfoss mouse lemur (M. danfossi) within the Anjajavy Reserve.\n\nTo demonstrate the reproducibility of our methods, we successfully performed our established molecular and analytical pipeline at two additional locations in Madagascar, where we also conducted two-day workshops at local higher-education Institutions to demonstrate the process from tissue samples to DNA sequencing. Ultimately, we show that a mobile genetics lab can provide reliable and expeditious results, become a powerful educational tool, and allow scientists to conduct genetic analyses, potentially allowing for rapid interventions under emergency conditions in situ.

genetics↗

bioRxiv2019

Comparative genomic analysis of the pheromone receptor Class 1 family (V1R) reveals extreme complexity in mouse lemurs (genus, Microcebus) and chromosomal hotspots across mammals

Sensory gene families are of special interest, both for what they can tell us about molecular evolution, and for what they imply as mediators of social communication. The vomeronasal type-1 receptors (V1Rs) have often been hypothesized as playing a fundamental role in driving or maintaining species boundaries given their likely function as mediators of intraspecific mate choice, particularly in nocturnal mammals. Here, we employ a comparative genomic approach for revealing patterns of V1R evolution within primates, with a special focus on the small-bodied nocturnal mouse and dwarf lemurs of Madagascar (genera Microcebus and Cheirogaleus, respectively). By doubling the existing genomic resources for strepsirrhine primates (i.e., the lemurs and lorises), we find that the highly-speciose and morphologically-cryptic mouse lemurs have experienced an elaborate proliferation of V1Rs that we argue is functionally related to their capacity for rapid lineage diversification. Contrary to a previous study that found equivalent degrees of V1R diversity in diurnal and nocturnal lemurs, our study finds a strong correlation between nocturnality and V1R elaboration, with nocturnal lemurs showing elaborate V1R repertoires and diurnal lemurs showing less diverse repertoires. Recognized subfamilies among V1Rs show unique signatures of diversifying positive selection, as might be expected if they have each evolved to respond to specific stimuli. Further, a detailed syntenic comparison of mouse lemurs with mouse (genus Mus) and other mammalian outgroups shows that orthologous mammalian subfamilies, predicted to be of ancient origin, tend to cluster in a densely populated region across syntenic chromosomes that we refer to as V1R \"hotspots.\"

genomics↗

bioRxiv2019

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

Madagascars biodiversity is notoriously threatened by deforestation and climate change. Many of these organisms are rare, cryptic, and severely threatened, making population-level sampling unrealistic. Such is the case with Madagascars dwarf lemurs (genus Cheirogaleus), the only obligate hibernating primate. We here apply comparative genomic approaches to generate the first genome-wide estimates of genetic diversity within dwarf lemurs. We generate a reference genome for the fat-tailed dwarf lemur, Cheirogaleus medius, and use this resource to facilitate analyses of high-coverage (~30x) genome sequences for wild-caught individuals representing species: C. sp. cf. medius, C. major, C. crossleyi and C. sibreei. This study represents the largest contribution to date of novel genomic resources for Madagascars lemurs. We find concordant phylogenetic relationships among the four lineages of Cheirogaleus across most of the genome, and yet detect a number of discordant genomic regions consistent with ancient admixture. We hypothesized that these regions could have resulted from adaptive introgression related to hibernation, indeed finding that genes associated with hibernation are present, though most significantly, that gene ontology categories relating to transcription are over-represented. We estimate levels of heterozygosity and find particularly low levels in an individual sampled from an isolated population of C. medius that we refer to as C. sp. cf. medius. Results are consistent with a recent decline in effective population size, which is evident across species. Our study highlights the power of comparative genomic analysis for identifying species and populations of conservation concern, as well as for illuminating possible mechanisms of adaptive phenotypic evolution.

genomics↗