Extinct Lemurs Research Articles

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) and other extraordinary Malagasy megafauna that survived 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 subtropical environments, technical advances have enabled the recovery of ancient DNA from some Malagasy subfossil specimens. Here, we present a nuclear genome sequence (∼2× coverage) for one of the largest extinct lemurs, the koala lemur Megaladapis edwardsi (∼85 kg). To support the testing of key phylogenetic and evolutionary hypotheses, we also generated high-coverage nuclear genomes for two extant lemurs, Eulemur rufifrons and Lepilemur mustelinus, and we aligned these sequences with previously published genomes for three other extant lemurs and 47 nonlemur 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 an extant folivore (a colobine monkey) and an herbivore (horse) in genes encoding proteins that function in plant toxin biodegradation 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.

Strontium Isotopes Support Small Home Ranges for Extinct Lemurs

Among mammals, including anthropoid primates, the primary factors that affect mobility are body size (larger-bodied species move more than smaller ones), diet (frugivores and trophic omnivores are more mobile than folivores), and habit (terrestrial taxa have larger home ranges than arboreal ones). If similar factors hold for Lemuriformes, we would expect large-bodied (particularly frugivorous) extinct lemurs to have been more mobile than smaller-bodied (particularly folivorous) extant species. Yet multiple lines of evidence (e.g., low Retzius Periodicities, small semicircular canal size, small relative brain size) suggest that extinct lemurs were relatively inactive. If so, they may have had relatively small home ranges, perhaps on par with smaller-bodied extant lemurs. We used strontium isotopes (87Sr/86Sr), which vary spatially primarily as a function of geology, to compare mobility for eight lemur genera: Eulemur, Lemur, Lepilemur and Propithecus (extant), and Archaeolemur, Megaladapis, Pachylemur and Palaeopropithecus (extinct). Subfossils came from two sites: Ankilitelo/Mikoboka, a series of sinkholes in a limestone plateau, and Ampasambazimba, a wetland underlain by a variety of igneous and metamorphic rocks. Within either site, we expected more mobile taxa to exhibit more variable 87Sr/86Sr, reflecting larger movement across a diversity of geologies. We found no differences in median 87Sr/86Sr or variance between extinct and extant lemurs at either site (Wilcoxon and Bartlett p>0.05 for all comparisons). There were apparent but insignificant differences among genera (Kruskal-Wallis and Bartlett p>0.05). Isotopic variability was greater at Ampasambazimba than at Ankilitelo/Mikoboka, reflecting differences in the underlying geology. One Palaeopropithecus from Ankilitelo/Mikoboka and one Eulemur from Ampasambazimba had unusually elevated 87Sr/86Sr. We suspect that both of these individuals were deposited at their respective sites by a predatory bird. These results demonstrate the value of 87Sr/86Sr for testing hypotheses related to the behavior of now-extinct species. Strontium isotopes support low mobility for extinct lemurs, and suggest that Lemuriformes as a whole differ from anthropoids in having relatively depressed basal metabolism and reduced activity levels. These traits reduce energetic expenditure, and likely developed in response to Madagascar’s harsh environments. However, small home ranges also make lemurs more vulnerable to extinction.

A new late Pleistocene subfossil site (Tsaramody, Sambaina basin, central Madagascar) with implications for the chronology of habitat and megafaunal community change on Madagascar's Central Highlands

ABSTRACTMadagascar is a complex ‘biodiversity hotspot’ with a rapidly dwindling biota. The Late Quaternary subfossil record includes many extinct species whose loss is attributed to natural climate change and human impacts. Investigation of the chronology of these events is challenging because few localities document pre‐Holocene communities not impacted by humans. Caves with extinct lemurs of large body size comprise some of Madagascar's richest subfossil sites, but provide only a limited window into the island's past. Open highland sites may have fewer primates, but may better document other megafauna, and allow the analysis of the role of the Central Highlands as refugia and as corridors for the dispersal of vertebrates before and after human arrival. Here we present a new subfossil site, Tsaramody (Sambaina basin, Central Madagascar), a high‐altitude wetland area that preserves a diverse late glacial and postglacial vertebrate community. Tsaramody bears testimony to fluctuations in the highland flora during the transition from glacial to postglacial conditions, and the composition of a highland vertebrate community before humans arrived. We compare its biota to those of other sites to begin to document the decline and disappearance of megafauna from some of Madagascar's open ecosystems – wetlands dominated by hippopotamuses and crocodylians. © 2019 John Wiley & Sons, Ltd.

Inferring the Diets of Extinct Giant Lemurs from Osteological Correlates of Muscle Dimensions.

The jaw adductor muscles of extinct mammals are often reconstructed to elucidate paleoecological relationships and to make broad comparisons among taxa. Muscle lever arms, bite load arms, muscle dimensions, and gape are often also reconstructed to better understand feeding. Several different approaches to these and related goals are discussed here. A protocol for reconstructing muscle dimensions and bite force using biomechanically informative skull measurements and osteological proxies of muscle dimensions is described and applied to a case study of subfossil Malagasy lemurs. The results of this case study show that most subfossil lemurs emphasized the masseter and medial pterygoid muscles over the temporalis. This supports the inference that these extinct lemurs depended heavily on tough food like leaves. Exceptions include signals of hard-object feeding in Archaeolemur that vary between A. majori and A. edwardsi. Reconstructions of soft-tissue and function are important for understanding past ecological relationships. Even those based on well-supported osteological proxies from extant analogues have limitations for making precise inferences. Anat Rec, 301:343-362, 2018. © 2018 Wiley Periodicals, Inc.

Cryptoprocta spelea (Carnivora: Eupleridae): What Did It Eat and How Do We Know?

The extent to which Madagascar’s Holocene extinct lemurs fell victim to nonhuman predators is poorly understood. Madagascar’s Holocene predator guild included several now-extinct species, i.e., crocodiles, carnivorans, and raptors. Here we focus on mammalian carnivory, specifically the roles of Cryptoprocta spelea and its still-extant but smaller-bodied sister taxon, C. ferox, the fosa. Cryptoprocta spelea was the largest carnivoran on Madagascar during the Quaternary. We ask whether some extinct lemurs exceeded the upper prey-size limits of C. spelea. We use univariate and multivariate phylogenetic generalized least squares regression models to re-evaluate the likely body mass of C. spelea. Next, we compare characteristics of the forelimb bones of C. ferox and C. spelea to those of other stealth predators specializing on small, mixed, and large-bodied prey. Finally, we examine humeri, femora, crania, and mandibles of extinct lemurs from six sites in four ecoregions of Madagascar to identify damage likely made by predators. We test the relative prevalence of carnivory by mammals, raptors, and crocodiles at different sites and ecoregions. Our data reveal that crocodiles, raptors, and the largest of Madagascar’s mammalian predators, C. spelea, all preyed on large lemurs. Cryptoprocta opportunistically consumed lemurs weighing up to ~85 kg. Its forelimb anatomy would have facilitated predation on large-bodied prey. Social hunting may have also enhanced the ability of C. spelea to capture large, arboreal primates. Cryptoprocta carnivory is well represented at cave and riverine sites and less prevalent at lake and marsh sites, where crocodylian predation dominates.

Testing the adaptive radiation hypothesis for the lemurs of Madagascar.

Lemurs, the diverse, endemic primates of Madagascar, are thought to represent a classic example of adaptive radiation. Based on the most complete phylogeny of living and extinct lemurs yet assembled, I tested predictions of adaptive radiation theory by estimating rates of speciation, extinction and adaptive phenotypic evolution. As predicted, lemur speciation rate exceeded that of their sister clade by nearly twofold, indicating the diversification dynamics of lemurs and mainland relatives may have been decoupled. Lemur diversification rates did not decline over time, however, as predicted by adaptive radiation theory. Optimal body masses diverged among dietary and activity pattern niches as lineages diversified into unique multidimensional ecospace. Based on these results, lemurs only partially fulfil the predictions of adaptive radiation theory, with phenotypic evolution corresponding to an ‘early burst’ of adaptive differentiation. The results must be interpreted with caution, however, because over the long evolutionary history of lemurs (approx. 50 million years), the ‘early burst’ signal of adaptive radiation may have been eroded by extinction.

Phylogeny and Divergence Times of Lemurs Inferred with Recent and Ancient Fossils in the Tree.

Paleontological and neontological systematics seek to answer evolutionary questions with different data sets. Phylogenies inferred for combined extant and extinct taxa provide novel insights into the evolutionary history of life. Primates have an extensive, diverse fossil record and molecular data for living and extinct taxa are rapidly becoming available. We used two models to infer the phylogeny and divergence times for living and fossil primates, the tip-dating (TD) and fossilized birth-death process (FBD). We collected new morphological data, especially on the living and extinct endemic lemurs of Madagascar. We combined the morphological data with published DNA sequences to infer near-complete (88% of lemurs) time-calibrated phylogenies. The results suggest that primates originated around the Cretaceous-Tertiary boundary, slightly earlier than indicated by the fossil record and later than previously inferred from molecular data alone. We infer novel relationships among extinct lemurs, and strong support for relationships that were previously unresolved. Dates inferred with TD were significantly older than those inferred with FBD, most likely related to an assumption of a uniform branching process in the TD compared with a birth-death process assumed in the FBD. This is the first study to combine morphological and DNA sequence data from extinct and extant primates to infer evolutionary relationships and divergence times, and our results shed new light on the tempo of lemur evolution and the efficacy of combined phylogenetic analyses.

Why all those spines? Anachronistic defences in the Didiereoideae against now extinct lemurs

Plants evolve physical defences, such as spines, against browsing herbivores. However, in some cases, these defences may be anachronistic because the principal consumers of protected parts of the plant are extinct. In such cases, there may be few extant species consuming heavily defended resources. Here we examine the spiny defences of Madagascar’s endemic Didiereoideae, and ask whether they may be anachronistic. To accomplish this aim, we reviewed the literature to determine which species consume these plants today, and then used stable isotope biogeochemistry to determine who may have exploited Didiereoideae in the recent past. There are four major groups of browsers that are now extinct in Madagascar: giant lemurs, elephant birds (Aepyornis and Mullerornis: Aepyornithidae), pygmy hippopotamuses (Hippopotamus) and giant tortoises (Aldabrachelys: Testudinidae). Each group was evaluated for isotopic evidence of didiereoid plant consumption. Given the structure of members of this plant clade (especially Alluaudia), we predicted that lemurs would be their most important consumers. Three extant lemur species consume Didiereoideae. Several of the extinct lemurs, particularly Hadropithecus stenognathus, may have relied heavily on these spiny plants. None of the non-lemur megafaunal browsers (elephant birds, hippopotamuses and giant tortoises) were important consumers of Didiereoideae.

Evidence for Dietary Niche Separation Based on Infraorbital Foramen Size Variation among Subfossil Lemurs

The size of the infraorbital foramen (IOF) has been used in drawing both phylogenetic and ecological inferences regarding fossil taxa. Within the order Primates, frugivores have relatively larger IOFs than folivores or insectivores. This study uses relative IOF size in lemurs to test prior trophic inferences for subfossil lemurs and to explore the pattern of variation within and across lemur families. The IOFs of individuals belonging to 12 extinct lemur species were measured and compared to those of extant Malagasy strepsirhines. Observations matched expectations drawn from more traditional approaches (e.g. dental morphology and microwear, stable isotope analysis) remarkably well. We confirm that extinct lemurs belonging to the families Megaladapidae and Palaeopropithecidae were predominantly folivorous and that species belonging to the genus Pachylemur (Lemuridae) were frugivores. Very high values for relative IOF area in Archaeolemur support frugivory but are also consistent with omnivory, as certain omnivores use facial touch cues while feeding. These results provide additional evidence that the IOF can be used as an informative osteological feature in both phylogenetic and paleoecological interpretations of the fossil record.

A glance to the past: subfossils, stable isotopes, seed dispersal, and lemur species loss in Southern Madagascar

The Spiny Thicket Ecoregion (STE) of Southern and southwestern Madagascar was recently home to numerous giant lemurs and other "megafauna," including pygmy hippopotamuses, giant tortoises, elephant birds, and large euplerid carnivores. Following the arrival of humans more than 2,000 years ago, dramatic extinctions occurred. Only one-third of the lemur species which earlier occupied the STE survive today; other taxa suffered even greater losses. We use stable isotope biogeochemistry to reconstruct past diets and habitat preferences of the recently extinct lemurs of the STE. We show that the extinct lemurs occupied a wide range of niches, often distinct from those filled by coeval non-primates. Many of the now-extinct lemurs regularly exploited habitats that were drier than the gallery forests in which the remaining lemurs of this ecoregion are most often protected and studied. Most fed predominantly on C3 plants and some were likely the main dispersers of the large seeds of native C3 trees; others included CAM and/or C4 plants in their diets. These new data suggest that the recent extinctions have likely had significant ecological ramifications for the communities and ecosystems of Southern and southwestern Madagascar.

“Life history space”: A multivariate analysis of life history variation in extant and extinct Malagasy lemurs

Studies of primate life history variation are constrained by the fact that all large-bodied extant primates are haplorhines. However, large-bodied strepsirrhines recently existed. If we can extract life history information from their skeletons, these species can contribute to our understanding of primate life history variation. This is particularly important in light of new critiques of the classic "fast-slow continuum" as a descriptor of variation in life history profiles across mammals in general. We use established dental histological methods to estimate gestation length and age at weaning for five extinct lemur species. On the basis of these estimates, we reconstruct minimum interbirth intervals and maximum reproductive rates. We utilize principal components analysis to create a multivariate "life history space" that captures the relationships among reproductive parameters and brain and body size in extinct and extant lemurs. Our data show that, whereas large-bodied extinct lemurs can be described as "slow" in some fashion, they also varied greatly in their life history profiles. Those with relatively large brains also weaned their offspring late and had long interbirth intervals. These were not the largest of extinct lemurs. Thus, we distinguish size-related life history variation from variation that linked more strongly to ecological factors. Because all lemur species larger than 10 kg, regardless of life history profile, succumbed to extinction after humans arrived in Madagascar, we argue that large body size increased the probability of extinction independently of reproductive rate. We also provide some evidence that, among lemurs, brain size predicts reproductive rate better than body size.

Une nouvelle espèce de lémurien géant subfossile du Nord-Ouest de Madagascar ( Palaeopropithecus kelyus, Primates)

For more than 20 years, a species of Palaeopropithecus has been suspected in the North-West of Madagascar. New discoveries in breccia from the sites of Belobaka and Ambongonambakoa permit us to describe the dental morphology of a new species, with a very developed parastyle and a mesostyle. This morphology is close to that which is found in the genus Propithecus. This small sized Palaeopropithecus could probably chew little bits of harder food than the two larger species. The description of this new species occurs 100 years after the other two, and suggests a greater diversity of Palaeopropithecus, extinct lemurs of large size and moving in a suspended manner like the South-American sloth.

The antiquity of Madagascar’s grasslands and the rise of C4 grassy biomes

AbstractAim Grasslands and savannas, which make up > 75% of Madagascar’s land area, have long been viewed as anthropogenically derived after people settled on the island c. 2 ka. We investigated this hypothesis and an alternative – that the grasslands are an insular example of the post‐Miocene spread of C4 grassy biomes world‐wide.Location Madagascar, southern Africa, East Africa.Methods We compared the number of C4 grass genera in Madagascar with that in southern and south‐central African floras. If the grasslands are recent we would expect to find fewer species and genera in Madagascar relative to Africa and for these species and genera to have very wide distribution ranges in Madagascar. Secondly, we searched Madagascan floras for the presence of endemic plant species or genera restricted to grasslands. We also searched for evidence of a grassland specialist fauna with species endemic to Madagascar. Plant and animal species endemic to C4 grassy biomes would not be expected if these are of recent origin.Results Madagascar has c. 88 C4 grass genera, including six endemic genera. Excluding African genera with only one or two species, Madagascar has 86.6% of southern Africa’s and 89.4% of south‐central Africa’s grass genera. C4 grass species make up c. 4% of the flora of both Madagascar and southern Africa and species : genus ratios are similar (4.3 and 5.1, respectively). Turnover of grasses along geographical gradients follows similar patterns to those in South Africa, with Andropogoneae dominating in mesic biomes and Chlorideae in semi‐arid grassy biomes. At least 16 monocot genera have grassland members, many of which are endemic to Madagascar. Woody species in frequently burnt savannas include both Madagascan endemics and African species. A different woody flora, mostly endemic, occurs in less frequently burnt grasslands in the central highlands, filling a similar successional niche to montane C4 grasslands in Africa. Diverse vertebrate and invertebrate lineages have grassland specialists, including many endemic to Madagascar (e.g. termites, ants, lizards, snakes, birds and mammals). Grassland use of the extinct fauna is poorly known but carbon isotope analysis indicates that a hippo, two giant tortoises and one extinct lemur ate C4 or CAM (crassulacean acid metabolism) plants.Main conclusions The diversity of C4 grass lineages in Madagascar relative to that in Africa, and the presence of plant and animal species endemic to Madagascan grassy biomes, does not fit the view that these grasslands are anthropogenically derived. We suggest that grasslands invaded Madagascar after the late Miocene, part of the world‐wide expansion of C4 grassy biomes. Madagascar provides an interesting test case for biogeographical analysis of how these novel biomes assembled, and the sources of the flora and fauna that now occupy them. A necessary part of such an analysis would be to establish the pre‐settlement extent of the C4 grassy biomes. Carbon isotope analysis of soil organic matter would be a feasible method for doing this.

Reconstruction of an extraordinary extinct primate from Madagascar

The minicontinent of Madagascar has been separated by 350 miles of ocean from its neighbor Africa for at least the past 120 million years, i.e., since long before the beginning of the Age of Mammals (1). As a result, the island's flora and fauna show extremely elevated levels of endemicity overall (2), and its native mammals show a curious combination of low diversity at the ordinal level with extraordinarily high diversity at lower taxonomic levels (3). Today, for example, Madagascar harbors an astonishing 30% of all primate families and some 21% of all primate genera (3), all of them represented nowhere else. Yet, high as these figures are, they would have been substantially higher a mere 2,000 years ago, before the arrival of Madagascar's first human inhabitants and the probably not coincidental extinction of a substantial proportion of the island's primate (lemur) fauna. In this issue of PNAS, Ryan et al. (4) report how new fossil discoveries and the use of computer-aided visualization techniques have significantly advanced our knowledge of cranial construction and body proportions in Hadropithecus, one of the most unusual of the recently extinct lemur genera.

Lemurs Making a Living in Unpredictable Environments

The lemurs of Madagascar have been the subject of field research for over five decades, the resulting considerable body of literature providing important new insights into the ecology, behavior, and evolution of Madagascar’s unique primate radiation. Lemurs: Ecology and Adaptation, edited by Lisa Gould and Michelle Sauther, represents a compilation of 20 chapters by 29 contributors who have conducted field work in Madagascar. The editors’ rationale for publishing this volume is to provide a single source for disseminating the results of new research on lemurs spanning the last fifteen years, including summaries of long-term research on well-known taxa as well as newly studied species. They believe these contributions will provide a better understanding of mammalian adaptations to harsh environments, many of which arise from anthropogenic causes. The book is divided into four sections covering lemur origins and ecology, the evolution of lemur traits, ecology and adaptation, and lemur adaptations to changing environments. Section One sets the evolutionary stage for the sections that follow, its three chapters providing reviews of lemur origins (Tattersall), the history of ecological studies of lemurs (Jolly and Sussman), and the ecology of recently extinct lemurs (Godfrey et al.). Malagasy lemurs are, not surprisingly, monophyletic, most likely derived, according to Tattersall, from a single forest canopy dwelling African strepsirrhine ancestor that colonized Madagascar during the early Tertiary. We learn from Godfrey et al.’s fascinating contribution that the ecological profiles of Madagascar’s primate communities were substantially different in the past than they are in the present, and that the special adaptations that are present in extinct forms most likely reflect the species’ energy conservation lifestyles. Jolly and Sussman catapult us into the present with a comprehensive and engagingly written review of the history of ecological studies of Malagasy lemurs, supplemented with a detailed summary of all lemur research conducted since the 1950s. Section Two is composed of three review and two data chapters focusing on the evolution of lemur traits. Cuozzo and Yamashita review recent data on the impact of ecology on teeth in extant lemurs and conclude (unsurprisingly) that tooth morphology is related to physical properties of food, yielding optimal designs for processing specific food. Curtis explores the proximate J Mammal Evol (2008) 15:215–217 DOI 10.1007/s10914-008-9073-y

MicroCT Analysis of Symphyseal Ontogeny in Archaeolemur

Previous analyses of symphyseal fusion in the extinct Malagasy lemur Archaeolemur identified several functional characteristics of joint morphology that vary postnatally (Ravosa and Simons in American Journal of Physical Anthropology 95:63–76, 1994). To complement that study, we used an imaging technique (microCT) that provides novel data on ontogenetic and local variation in biomineralization along the mandibular symphysis before complete ossification among adult Archaeolemur. Our sample of unfused symphyses comprised juveniles from the 2 earliest postnatal dental ages examined previously. We imaged each specimen (ca.18 μm volume elements) with slices parallel to the coronal plane, i.e., orthogonal to the joint articular surface. In ≤5 labiolingually equidistant joint sites, we collected 40 contiguous slices (18-μm intervals). Each of the 5 joint sites is represented by 1 slice, with biomineralization values sampled at 5 equidistant points along the articular surface and at 3 external cortical bone points. Our analysis of Archaeolemur indicates the presence of ontogenetic increases in bone mineral density accompanying increases in joint size and the number and distribution of symphyseal rugosities. Such postnatal changes are particularly marked for the middle of the joint presumed to lie adjacent to a degrading fibrocartilage pad. In Archaeolemur, labial regions of the symphysis ossify earlier and are likewise more biomineralized. Ontogenetic increases in symphyseal biomineralization, overall size, and fusion are consistent with elevated masticatory stresses owing to the postweaning shift to adult-like feeding behaviors. However, the labiolingual pattern of fusion and biomineralization in Archaeolemur appears related more to constraints on synostosis owing to the lingually located vascular supply characteristic of mammalian symphyses.

The secrets of lemur teeth

New tools are available for teasing out aspects of life-history variation among extinct species. Here we summarize research on the life histories of the extinct lemurs of Madagascar. There is a wide range of variation in dental developmental timing among these species, from among the most accelerated (Palaeopropithecus) to among the most prolonged (Hadropithecus) within the Order Primates. Rather than reflecting variation in body size, this diversity appears to relate to niche characteristics and encephalization.

Dental development in Megaladapis edwardsi (Primates, Lemuriformes): Implications for understanding life history variation in subfossil lemurs

Teeth grow incrementally and preserve within them a record of that incremental growth in the form of microscopic growth lines. Studying dental development in extinct and extant primates, and its relationship to adult brain and body size as well as other life history and ecological parameters (e.g., diet, somatic growth rates, gestation length, age at weaning), holds the potential to yield unparalleled insights into the life history profiles of fossil primates. Here, we address the absolute pace of dental development in Megaladapis edwardsi, a giant extinct lemur of Madagascar. By examining the microstructure of the first and developing second molars in a juvenile individual, we establish a chronology of molar crown development for this specimen (M 1 CFT = 1.04 years; M 2 CFT = 1.42 years) and determine its age at death (1.39 years). Microstructural data on prenatal M 1 crown formation time allow us to calculate a minimum gestation length of 0.54 years for this species. Postnatal crown and root formation data allow us to estimate its age at M 1 emergence (∼0.9 years) and to establish a minimum age for M 2 emergence (>1.39 years). Finally, using reconstructions or estimates (drawn elsewhere) of adult body mass, brain size, and diet in Megaladapis, as well as the eruption sequence of its permanent teeth, we explore the efficacy of these variables in predicting the absolute pace of dental development in this fossil species. We test competing explanations of variation in crown formation timing across the order Primates. Brain size is the best single predictor of crown formation time in primates, but other variables help to explain the variation.

Evidence of early butchery of giant lemurs in Madagascar

We report here definitive evidence of butchery, most probably associated with hunting, of giant extinct lemurs by early human settlers in Madagascar. Specimens of Palaeopropithecus ingens and Pachylemur insignis from two sites in southwestern Madagascar, Taolambiby and Tsirave, show classic signs of butchering. We compared these to the bones (also from Taolambiby) of butchered Propithecus verreauxi, a lemur still living in the region. The characteristics of the tool-induced extinct-lemur bone alterations (sharp cuts and chop marks near joints, oblique cuts along the shafts, spiral fractures, and percussion striae) suggest skinning, disarticulation, and filleting. Conclusive evidence of megafaunal modification by humans in Madagascar was limited previously to a few hippo and elephant bird bones and one extinct aye-aye tooth. New evidence comes not from archaeological sites, but from specimens collected in the early 1900s, without stratigraphic records, at “subfossil” sites (i.e., sites renowned for their late Pleistocene or Holocene fossils, often lacking human artifacts). Whereas these are hardly the most ideal samples for analysis of this kind, careful scrutiny of the characteristics of the cut marks has allowed us to document butchery beyond any reasonable doubt. One bone with definitive cut marks has been dated to the very earliest part of the human period in Madagascar. Continued, careful research on the bones in subfossil collections is warranted.

Ancient DNA from giant extinct lemurs confirms single origin of Malagasy primates.

The living Malagasy lemurs constitute a spectacular radiation of >50 species that are believed to have evolved from a common ancestor that colonized Madagascar in the early Tertiary period. Yet, at least 15 additional Malagasy primate species, some of which were relative giants, succumbed to extinction within the past 2,000 years. Their existence in Madagascar is recorded predominantly in its Holocene subfossil record. To rigorously test the hypothesis that all endemic Malagasy primates constitute a monophyletic group and to determine the evolutionary relationships among living and extinct taxa, we have conducted an ancient DNA analysis of subfossil species. A total of nine subfossil individuals from the extinct genera Palaeopropithecus and Megaladapis yielded amplifiable DNA. Phylogenetic analysis of cytochrome b sequences derived from these subfossils corroborates the monophyly of endemic Malagasy primates. Our results support the close relationship of sloth lemurs to living indriids, as has been hypothesized on morphological grounds. In contrast, Megaladapis does not show a sister-group relationship with the living genus Lepilemur. Thus, the classification of the latter in the family Megaladapidae is misleading. By correlating the geographic location of subfossil specimens with relative amplification success, we reconfirm the global trend of increased success rates of ancient DNA recovery from nontropical localities.