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Hibernation is a widespread metabolic strategy among mammals for surviving periods of food scarcity. During hibernation, animals naturally alternate between metabolically depressed torpor bouts and energetically expensive arousals without ill effects. As a result, hibernators are promising models for investigating mechanisms that buffer against cellular stress, including telomere protection and restoration. In non-hibernators, telomeres, the protective structural ends of chromosomes, shorten with age and metabolic stress. In temperate hibernators, however, telomere shortening and elongation can occur in response to changing environmental conditions and associated metabolic state. We investigate telomere dynamics in a tropical hibernating primate, the fat-tailed dwarf lemur ( Cheirogaleus medius ). In captivity, these lemurs can hibernate when maintained under cold temperatures (11–15 °C) with limited food provisioning. We study telomere dynamics in eight fat-tailed dwarf lemurs at the Duke Lemur Center, USA, from samples collected before, during, and after the hibernation season and assayed via qPCR. Contrary to our predictions, we found that telomeres were maintained or even lengthened during hibernation, but shortened immediately thereafter. During hibernation, telomere lengthening was negatively correlated with time in euthermia. Although preliminary in scope, our findings suggest that there may be a preemptive, compensatory mechanism to maintain telomere integrity in dwarf lemurs during hibernation. Nevertheless, telomere shortening immediately afterward may broadly result in similar outcomes across seasons. Future studies could profitably investigate the mechanisms that offset telomere shortening within and outside of the hibernation season and whether those mechanisms are modulated by energy surplus or crises.

Primate encounter rates often vary throughout the year due to seasonal differences in activity, ecology, and behaviour. One notably extreme behaviour is continuous hibernation. Although a rare adaptation in primates, the dwarf lemurs of Madagascar (genus Cheirogaleus) enter obligate hibernation each year during the dry season, after spending the wet season consuming high-energy foods. Whilst seasonal changes in activity in some Cheirogaleus populations are well-known, many species remain little-studied, and there is no specific information on their encounter rates, nor when they enter and emerge from hibernation. This uncertainty critically affects reliable calculation of population density estimates for these highly threatened lemurs. In this study, we assessed how encounter rates of the fat-tailed dwarf lemur (C. medius) vary seasonally in the transitional forests of the Sahamalaza-Iles Radama National Park, northwest Madagascar, during a 4-year period. We established a system of line transects (N = 60) throughout our study area, on which we conducted distance sampling of C. medius. We then used our distance sampling data to calculate encounter rate and population density data. We found encounter rates of C. medius to be significantly higher during the wet season compared with the dry season. Furthermore, encounter rates of C. medius were particularly low from May–August. These results provide some evidence to suggest the time period that C. medius hibernate in Sahamalaza-Iles Radama National Park. These findings underpin the importance of careful study design when surveying threatened species with seasonal differences in activity, such as those that hibernate. This study also demonstrates the importance of species-specific behavioural data for accurate population density assessment, which is required to inform conservation action.

Abstract The gut microbiome can mediate host metabolism, including facilitating energy-saving strategies like hibernation. The dwarf lemurs of Madagascar (Cheirogaleus spp.) are the only obligate hibernators among primates. They also hibernate in the subtropics, and unlike temperate hibernators, fatten by converting fruit sugars to lipid deposits, torpor at relatively warm temperatures, and forage for a generalized diet after emergence. Despite these ecological differences, we might expect hibernation to shape the gut microbiome in similar ways across mammals. We, therefore, compare gut microbiome profiles, determined by amplicon sequencing of rectal swabs, in wild furry-eared dwarf lemurs (C. crossleyi) during fattening, hibernation, and after emergence. The dwarf lemurs exhibited reduced gut microbial diversity during fattening, intermediate diversity and increased community homogenization during hibernation, and greatest diversity after emergence. The Mycoplasma genus was enriched during fattening, whereas the Aerococcaceae and Actinomycetaceae families, and not Akkermansia, bloomed during hibernation. As expected, the dwarf lemurs showed seasonal reconfigurations of the gut microbiome; however, the patterns of microbial diversity diverged from temperate hibernators, and better resembled the shifts associated with dietary fruits and sugars in primates and model organisms. Our results thus highlight the potential for dwarf lemurs to probe microbiome-mediated metabolism in primates under contrasting conditions. Wild dwarf lemurs in Madagascar show seasonal reconfigurations of the gut microbiome across the annual hibernation cycle, with microbial diversity tracking the host’s reliance on dietary fruit sugars.

Conservation action, vital in biodiversity hotspots, depends on reliable data on endangered taxa. This is especially important for species that are morphologically cryptic and difficult to distinguish in the field. The dwarf lemurs of Madagascar ( Cheirogaleus spp.) exemplify these challenges: They are widespread but endangered, nocturnal, small‐sized, and cryptic. The genus is diverse, with nine described species and as many candidate species, falling into four distinct lineages (“medius,” “sibreei,” “crossleyi,” and “major”). Many protected areas in Madagascar harbor dwarf lemur populations that await genetic species confirmation. Here, we collated tissue samples from 30 individual dwarf lemurs in 10 forest sites collected by a network of collaborators over a decade. We sequenced the simple but diagnostic cytochrome‐b marker gene and placed samples into a curated database of > 200 published sequences. Except for an individual from the “sibreei” lineage in Marojejy that separated from close relatives farther south, our samples fell into described or candidate species, supporting geographic clustering within lineages. We identified two sites in the northeast that harbor different assemblages of species from three distinct lineages in sympatry. We confirmed the presence of C. crossleyi at sites across Madagascar's central highlands, considerably extending its known range, and posit that this is the dominant dwarf lemur of the highlands north of the Mangoky river. Although our results are limited in resolution and call for in‐depth genomics, we advocate for foundational field work, natural history exploration, and survey/sampling expeditions to generate the very data on which sophisticated genomics and computational methods rely. 保护行动对于生物多样性热点地区至关重要, 它依赖于濒危类群的可靠数据。这对于那些形态隐蔽 (morphologically cryptic) 且难以在野外区分的物种尤为重要。马达加斯加的鼠狐猴属 ( Cheirogaleus spp.) 正是这些挑战的典型代表:它们分布广泛但濒临灭绝, 且为夜行性、体型小且隐蔽的物种。该属具有多样性, 包括9个已描述物种和同样数量的候选物种, 分为四个独特的谱系 (“medius”、“sibreei”、“crossleyi”和“major”) 。马达加斯加的许多保护区内栖息着尚待遗传物种确认的鼠狐猴种群。在此, 我们整理了合作网络在十年间于10个森林位点采集的30只鼠狐猴个体的组织样本。我们对简单但具有诊断价值的细胞色素b (cytochrome‐b) 标记基因进行了测序, 并将样本放入包含200多条已发表序列的精选数据库中。除了来自马洛杰吉 (Marojejy) 的一只“sibreei”谱系个体与其南部近亲分离外, 我们的样本均归入已描述物种或候选物种, 支持了谱系内的地理聚类。我们在东北部确定了两个位点, 那里栖息着来自三个不同谱系的物种构成的不同同域分布组合。我们确认了克氏鼠狐猴 ( C. crossleyi ) 在马达加斯加中部高地多个位点的存在, 极大地扩展了其已知分布范围, 并推断这是Mangoky河以北高地的优势鼠狐猴物种。尽管我们的结果分辨率有限且需要深入的基因组学研究, 但我们提倡开展基础性的野外工作、自然史探索以及调查/采样考察, 以生成复杂基因组学和计算方法所依赖的基础数据。 Mifototra amin'ny tahirin‐kevitra azo antoka ny asa fiarovana, indrindra ho an'ireo karazan‐javamanan'aina akaiky ho lany tamingana, izay mitovy endrika ivelany kanefa sarotra avahana toy ireo Matavirambo eto Madagasikara ( Cheirogaleus spp.). Mavitrika amin'ny alina, mitovitovy endrika ivelany sy sarotra avahana izy ireo kanefa samihafa tarazo, na dia miparitaka amin'ny toerana maro eto Madagasikara aza. Misy karazana 9 ny Cheirogaleus spp. ary mitsinjara ho vondrona 4, “medius”, “sibreei”, “crossleyi”, ary “major”. Faritra arovana maro no hahitana ireo Matavirambo, saingy mila porofo ara‐poto‐tarazo ny fanammarinana ny taranaka misy azy ireo. Teto izahay dia nanangona santionana sela miisa 30 avy tamin'ireo Matavirambo miparitaka ao anatin'ny faritr'ala 10. Izany no tanteraka dia noho ny fiaraha‐miasa nisy teo amin ireo mpikaroka maro tao anatin'ny 10 taona. Nitsirika ny rindran‐damin'ny fototrin'ny aina tamin'ny fomba tsotra nefa azo antoka izahay ary niasa tamin'ny faritra cytochrome‐b. Ireo rindran‐damin'ny fototrin'ny aina ireo dia nalefa tao anaty ango‐kevitra mari‐pototra sy efa voamarina sahabo eo amin'ny 200 isa eo. Voamarina fa tafiditra amin'ny karazana na kandida ny ankamaroan'ny santionanay. Manaporofo izany fa misy famoriam‐piarahamonina araka ny jeografia ao amin'ireo fizarana, afa‐tsy ilay singa iray avy amin'ny fizarana “sibreei” ao Marojejy izay misaraka amin'ireo akaiky azy, izay voafaritra somary atsimo kokoa. Nahitana toerana roa any avaratra‐atsinanana izay samy mampiantrano karazana avy amin'ny fizarana (lignée) telo samihafa. Voamarina ihany koa fa C. crossleyi dia karazana hita matetika amin'ny faritra avo afovoan'i Madagasikara. Mivelatra kokoa noho izany ny toeramponenany satria hahitana azy ihany koa hatrany amin'ny faritra avaratry ny renirano Mangoky. Na dia voafetra aza ny vokatra nasehonay ary mitaky fikarohana ara‐pototarazo lalindalina kokoa, dia manamafy ny maha‐zava dehibe ny fitsidihana toerana isankarazany sy ny fangalana santionany. Ilaina ihany koa ny fanadihadiana ny tantaram‐piainana ara‐voajanahary eny ifotony hanampiana ireo fitsirihana/santionana mba hanangonana ny angon‐drakitra izay ivon'ny fikarohana ara‐pototarazo sy fikajiana manaraka ny toetr'andro. Species are the unit by which we count biodiversity and assess extinction risk. We therefore need to know which species live where. Assigning species in the wild is challenging when individuals look alike, and when they are small‐sized and nocturnal. This is the case for the dwarf lemurs of Madagascar. There are currently nine known species and several candidate species of dwarf lemurs that inhabit different forests in Madagascar. These lemurs are only identifiable by sequencing their DNA, and many sites in Madagascar await such genetic species confirmations. We use a diagnostic marker gene to confirm the dwarf lemur species at 10 sites for which prior data were sparse or inconclusive. We find that multiple dwarf lemur species inhabit the same forests in northeastern Madagascar. We also show that one species, the furry‐eared dwarf lemur, is exclusively found in very small, fragmented forests across the central highlands. While acknowledging our limitations, we advocate for additional field surveys to better delineate true species geographic distributions. This information can help answer questions about how these lemurs got there in the first place and whether they may be resilient or tolerant to impending climate and anthropogenic changes. Ny karazana no singa entina mandrefy ny karazan‐java‐anan'aina sy hanombanana ny tatao mety hahalany tamingana azy. Noho izany, zava‐dehibe ny fahalalàna mazava momba ny toerana misy ny karazana tsirairay. Sarotra anefa ny mamantatra ny karazana rehefa mitovy endrika ivelany sy samy mavitrika amin’ny alina izy ireo. Izany indrindra no zava‐misy amin’ny Mativirambo na dwarf lemurs eto Madagasikara. Amin’izao fotoana izao dia karazana 9 no efa voafaritra ara‐tsiansa, ary misy karazana kandida maromaro hafa fantatra fa monina amin’ny ala manerana an’i Madagasikara. Amin'ny ankapobeny dia amin'ny alalan'ny fandaharana ny rindran‐damin’ny fototrin'ny aina (ADN) ihany no ahafahana mamantatra tsara ireo Matavirambo ireo, ary mbola maro amin'ny toerana eto Madagasikara no tsy mbola manana fanamafisana ara‐pototarazo ny karazana misy. Mampiasa mari‐pototra ADN izahay mba hamantarana sy hanamafisana ny karazana Matavirambo amin'ny toerana 10 izay mbola tsy nisy ny angon‐drakitra hatramin’izay. Hitanay fa misy karazana Matavirambo maro monina anaty ala iray any avaratra atsinanan'i Madagasikara. Nasehonay ihany koa fa ny iray amin'ireo karazana, ny Matavirambo (furry‐eared dwarf lemurs), dia hita manokana amin'ny tsitokotokon’ala kely manodidina ny afovoan‐tany. Na dia nisy fetrany aza ny fikarohana natao, dia manentana ny hanaovana fitsirihana ifotony fanampiny izahay mba hahafahana mamantatra mazava kokoa ny fizaran‐toeran’ireo karazana. Ity fikarohana ity dia afaka manampy amin'ny famaliana ny fanontaniana ny amin’ny fomba nahatongavan'ireo Matavirambo ireo tany amin'ireny faritra ireny, sy ny fanombanana ny fahazakan’izy ireo izay mety fiovaovan'ny toetrandro sy ny fiantraikan’ny tsindry ataon’ny olombelona. We confirmed the species identity of 30 dwarf lemurs inhabiting 10 protected areas across Madagascar using a mitochondrial marker gene, cytochrome‐b. We identified a large range expansion for the furry‐eared dwarf lemur ( Cheirogaleus crossleyi ) across multiple sites in the central highlands and posit that this species is likely the dominant and only dwarf lemur in this understudied region. We revealed centers of sympatry in the northeast, with different assemblages of three species of dwarf lemur inhabiting Marojejy National Park and the Tsihomanaomby Protected Area. Nohamafisinay ny maha‐izy azy (karazany) ny Matavirambo (dwarf lemurs) 30 hita ao amin'ny Faritra arovana 10 manerana an'i Madagasikara, tamin'ny alalan'ny fampiasana ny mpamaritra foto‐tarazo ao amin'ny mitochondrie, dia ny cytochrome‐b. Hitanay fa mivelatra midadasika ny faritra misy ny Cheirogaleus crossleyi amin’ny faritra afovoan‐tany ary azo inoana fa io karazana io no tena betsaka amin’ireto faritra mbola tsy nojerena lalina ireto. Nasehonay fa misy faritra iarahan’ny karazana samihafa miaina (centres de sympatrie) any amin'ny faritra avaratra atsinanana, miaraka amin'ny vondron'ireo karazana Matavirambo telo samihafa monina ao amin'ny Valan‐javaboary Marojejy sy ny Faritra Arovana Tsihomanaomby. 物种是我们统计生物多样性和评估灭绝风险的单位。因此, 我们需要了解哪些物种生活在哪里。当个体外貌相似, 且体型小、夜间活动时, 在野外确定物种具有挑战性。马达加斯加的鼠狐猴就是这种情况。目前已知有9种鼠狐猴和几个候选物种栖息在马达加斯加的不同森林中。这些狐猴只能通过DNA测序来识别, 马达加斯加的许多地点正等待这种遗传物种确认。我们使用一种诊断性标记基因来确认10个地点的鼠狐猴物种, 这些地点之前的数据稀缺或不确凿。我们发现多种鼠狐猴栖息在马达加斯加东北部的同一片森林中。我们还表明, 有一个物种, 即毛耳鼠狐猴 (furry‐eared dwarf lemur), 仅发现于中部高地非常小且破碎化的森林中。在承认我们的局限性的同时, 我们提倡进行更多的野外调查, 以更好地划定真实的物种地理分布。这些信息有助于回答这些狐猴最初是如何到达那里的, 以及它们是否能够抵御或耐受即将到来的气候和人为变化。 实践者要点 我们利用线粒体标记基因细胞色素b (cytochrome‐b), 确认了栖息在马达加斯加全境10个保护区的30只鼠狐猴的物种身份。 我们确定了毛耳鼠狐猴 (Cheirogaleus crossleyi) 在中部高地多个位点的分布范围大幅扩展, 并推断该物种可能是这一研究不足区域的主要 (且唯一) 鼠狐猴物种。 我们揭示了东北部的同域分布中心, 在马洛杰吉国家公园 (Marojejy National Park) 和Tsihomanaomby保护区栖息着由三种鼠狐猴构成的不同组合

Most studies of wildlife gut microbiotas understandably rely on feces to approximate consortia along the gastrointestinal tract. We therefore compared microbiome structure and predicted metagenomic function in stomach, small intestinal, cecal, and colonic samples from 52 lemurs harvested during routine necropsies. The lemurs represent seven genera ( Cheirogaleus , Daubentonia , Varecia , Hapalemur , Eulemur , Lemur , Propithecus ) characterized by diverse feeding ecologies and gut morphologies. In particular, the hosts variably depend on fibrous foodstuffs and show correlative morphological complexity in their large intestines. Across host lineages, microbiome diversity, variability, membership, and function differed between the upper and lower gut, reflecting regional tradeoffs in available nutrients. These patterns related minimally to total gut length but were modulated by fermentation capacity (i.e., the ratio of small to large intestinal length). Irrespective of feeding strategy, host genera with limited fermentation capacity harbored more homogenized microbiome diversity along the gut, whereas those with expanded fermentation capacity harbored cecal and colonic microbiomes with greater diversity and abundant fermentative Ruminococcaceae taxa. While highlighting the value of curated sample repositories for retrospective comparisons, our results confirm that the need to survive on fibrous foods, either routinely or in hypervariable environments, can shape the morphological and microbial features of the lower gut.

Ecological niches are the environmental conditions under which an organism can maintain viable populations. A detailed understanding of an organisms’ ecological niche can provide information on its taxonomy and biogeography, and ecological niche modelling allows researchers to investigate how closely-related species are able to coexist. Ecological niche models also enable conservationists to determine species’ habitat requirements, map distributions, and assess threats. We used this approach to investigate the conservation biogeography of the dwarf lemurs (genus Cheirogaleus), a group of cryptic, nocturnal primates endemic to Madagascar. Using climatic and vegetation-related variables, we constructed ecological niche models for three species to investigate niche overlap among taxa. We also constructed maps of the availability of forest habitat, and we assessed anthropogenic risk and protection. Our ecological niche models and background tests indicated that each of the three analysed Cheirogaleus species occupies distinct environmental space. The area of suitable habitat (realized niche) varied interspecifically (28,889–41,934 km2). This also was mirrored by variation in the percentage of each species’ realized niche within protected areas (20,065–25,266 km2) and near anthropogenic features (5,744–16,999 km2). Our results support the 2020 taxonomy of the dwarf lemurs recognised by the IUCN Red List and provides information on their biogeography. Furthermore, our ecological niche models have highlighted that the habitat of some dwarf lemur species, such as C. crossleyi, are more threatened than other species, such as C. medius and C. major, and these species require urgent conservation attention.

Fat-tailed dwarf lemurs (Cheirogaleus medius), primates endemic to Madagascar, are obligate hibernators that form stable, lifelong pairs in the wild. Given the temporal constraints imposed by seasonal hibernation, infant dwarf lemurs must grow, develop, and wean within the first two months of life. Maternal as well as paternal infant care, observed in the wild, has been deemed critical for infant survival. Given the importance of fathers’ involvement in early infant care, we expect this behavior to persist even under captive conditions. At the Duke Lemur Center, in Durham NC, we observed two families of fat-tailed dwarf lemurs and focused on the behavior of adult males within the first two months of the infants’ lives. We report evidence of paternal involvement, including babysitting, co-feeding, grooming, accompanying, and leading infants, consistent with observations from the wild. As expected, paternal babysitting decreased as infants gained independence, while co-feeding increased. Supplemental anecdotes, video recorded by observers, also highlight clear cases of involvement by both parents, and even older siblings, in safeguarding and socializing new infants. We argue that maintaining captive fat-tailed dwarf lemur populations under socially and ecologically relevant conditions facilitates the full expression of physiological and behavioral repertoires. Most importantly, it also allows dwarf lemurs to realize their species’ potential and become robust proxies of their wild kin.

Hibernation is a fascinating physiological phenomenon that dramatically reduces metabolism, resulting in a large deviation of body temperature (Tb) from the homeothermic range in mammals. Although high-resolution and long-term Tb recording in wild or laboratory animals has become possible through bio-logging, few standardized methods for analysing the details of hibernation patterns are available, making it difficult to reproduce and compare the results across different studies and species. To facilitate the analysis of Tb patterns and aid hibernation research, we developed an open-source program, tools of hibernation measurement and interpretation (TOHMIN). As a proof of concept, we analysed a Tb dataset from pilot studies on the effects of distinct diets on hibernation patterns and differences in hibernation patterns between sexes in a mammalian hibernator, the Syrian hamster (Mesocricetus auratus), and found previously undetectable fine-scale differences in hibernation patterns. In addition, we demonstrated that TOHMIN can successfully analyse hibernation patterns in the 13-lined ground squirrel (Ictidomys tridecemlineatus) and the fat-tailed dwarf lemur (Cheirogaleus medius) both maintained under captive conditions. Furthermore, our tool helped analyse torpor patterns in mice (Mus musculus) upon restricted feeding. Thus, TOHMIN facilitates studies that assess the effects of various experimental manipulations on hibernation and torpor phenotypes (hibernation is a form of torpor) in mammals.

Speciation begins when populations become genetically separated through a substantial reduction in gene flow, and it is at this point that a genetically cohesive set of populations attain the sole property of species: the independent evolution of a population-level lineage. The comprehensive delimitation of species within biodiversity hotspots, regardless of their level of divergence, is important for understanding the factors that drive the diversification of biota and for identifying them as targets for conservation. However, delimiting recently diverged species is challenging due to insufficient time for the differential evolution of characters--including morphological differences, reproductive isolation, and gene tree monophyly--that are typically used as evidence for separately evolving lineages. In this study, we assembled multiple lines of evidence from the analysis of mtDNA and nDNA sequence data for the delimitation of a high diversity of cryptically diverged population-level mouse lemur lineages across the island of Madagascar. Our study uses a multi-faceted approach that applies phylogenetic, population genetic, and genealogical analysis for recognizing lineage diversity and presents the most thoroughly sampled species delimitation of mouse lemur ever performed. The resolution of a large number of geographically defined clades in the mtDNA gene tree provides strong initial evidence for recognizing a high diversity of population-level lineages in mouse lemurs. We find additional support for lineage recognition in the striking concordance between mtDNA clades and patterns of nuclear population structure. Lineages identified using these two sources of evidence also exhibit patterns of population divergence according to genealogical exclusivity estimates. Mouse lemur lineage diversity is reflected in both a geographically fine-scaled pattern of population divergence within established and geographically widespread taxa, as well as newly resolved patterns of micro-endemism revealed through expanded field sampling into previously poorly and well-sampled regions.