Andrea L. Baden

Primate cranial diversity

Many studies in primate and human evolution focus on aspects of cranial morphology to address issues of systematics, phylogeny, and functional anatomy. However, broad analyses of cranial diversity within Primates as an Order are notably absent. In this study, we present a 3D geometric morphometric analysis of primate cranial morphology, providing a multivariate comparison of the major patterns of cranial shape change during primate evolution and quantitative assessments of cranial diversity among different clades. We digitized a set of 18 landmarks designed to capture overall cranial shape on male and female crania representing 66 genera of living primates. The landmark data were aligned using a Generalized Procrustes Analysis and then subjected to a principal components analysis to identify the major axes of cranial variation. Cranial diversity among clades was compared using multivariate measurements of variance. The first principal component axis reflects differences in cranial flexion, orbit size and orientation, and relative neurocranial volume. In general, it separates strepsirrhines from anthropoids. The second axis reflects differences in relative cranial height and snout length and primarily describes differences among anthropoids. Eulemur, Mandrillus, Pongo, and Homo are among the extremes in cranial shape. Anthropoids, catarrhines, and haplorhines show a higher variance than prosimians or strepsirrhines. Hominoids show the highest variance in cranial shape among extant primate clades, and much of this diversity is driven by the unique cranium of Homo sapiens.

Frugivory in four sympatric lemurs: implications for the future of Madagascar's forests.

Although some conservationists accept that not all species can be saved, we illustrate the difficulty in deciding which species are dispensable. In this article, we examine the possibility that the integrity of a forest relies on its entire faunal assemblage. In Madagascar, one faunal group, the lemurs, accounts for the greatest biomass and species richness among frugivores. For example, 7 of the 13 sympatric lemur species in Madagascars eastern rainforests consume primarily fruit. Because of this, we suggest that some tree species may rely heavily on particular lemur taxa for both seed dispersal and germination. In Ranomafana National Park, the diets for four of the day‐active lemur frugivores have been documented during annual cycles over a 5‐year period. We predicted that, although the fruit of some plant taxa would be exploited by multiple lemur species, the fruit of others would be eaten by one lemur species alone. Analyses reveal that while lemurs overlap in a number of fruit taxa exploited, 46% (16/35) of families and 56% (29/52) of genera are eaten exclusively by one lemur species. We, therefore, predict local changes in forest composition and structure if certain of these lemur species are eliminated from a forest owing to hunting, disease, or habitat disturbance. We also suggest that this result may be of global significance because carbon sequestration by the tropical forests in Madagascar may be reduced as a result of this predicted change in forest composition. Am. J. Primatol. 73:585–602, 2011.

Long-Term Lemur Research at Centre Valbio, Ranomafana National Park, Madagascar

We present findings from 25 years of studying 13 species of sympatric primates at Ranomafana National Park, Madagascar. Long-term studies have revealed that lemur demography at Ranomafana is impacted by climate change, predation from raptors, carnivores, and snakes, as well as habitat disturbance. Breeding is seasonal, and each species (except Eulemur rubriventer) gives birth synchronously to be able to wean before winter. Infant mortality is high (30–70%) and partly due to infanticide in Propithecus edwardsi,and perhaps Varecia variegata. Diurnal lemurs can live beyond 30 years in the wild and most females reproduce until death. Small-bodied Microcebus rufuslive up to 9 years without signs of senescence. Prolemur simusmigrates in search of new bamboo and mates, and related V. variegatamothers park their multiple offspring in “kindergartens,” protected by others while mothers forage. Interference competition among sympatric lemurs occurs. Anthropogenic factors, such as past selective logging and climate change may influence the declining density of E. rufifrons, P. simus, and P. edwardsiwhile not affecting the density of pair-living species.

Infant parking and nesting, not allomaternal care, influence Malagasy primate life histories

Allomaternal care is a rare, though phylogenetically widespread, mammalian infant care strategy. Among primates, the effects of allomaternal care are marked; its presence correlates with faster infant growth, younger age at weaning, and shorter interbirth intervals. Recent comparative research has found that such fertility benefits are absent in other mammals and are thus unique to primates. In large part because data describing lemur allomaternal care were lacking, the reproductive advantages of allomaternal care have never been demonstrated in Malagasy strepsirrhines. Using newly available data and rigorous phylogenetic methods, we extend this hypothesis to strepsirrhines and test whether allomaternal care in lemurs confers similar maternal reproductive benefits. Contrary to expectations, the presence of allomaternal care did not significantly impact lemur reproductive output; we did not find relationships between allomaternal care and either fetal or postnatal growth rates or interbirth intervals. Rather, infant parking and nesting, strategies employed primarily by litter-bearing species, were positively associated with faster fetal and postnatal infant growth, while nesting was negatively associated with interbirth interval. Thus, although each form of haplorrhine allomaternal care is also observed in Malagasy primates, the effects that these behaviors have on female reproductive output more closely resemble nonprimate mammals. We suggest that Malagasy strepsirrhines may not equally benefit from allomaternal care compared to haplorrhines because reproductive rates are less flexible and allomaternal care may instead increase infant survival in Madagascar’s harsh and unpredictable environment. Our study has significant implications for understanding the evolution of infant care and developmental trajectories in mammals.

Reproductive Strategies and Infant Care in the Malagasy Primates

The old African proverb, “It takes a village to raise a child,” may extend well beyond the collective effort attributed to human child rearing strategies. In fact, allomaternal care is taxonomically widespread, particularly among mammalian taxa (e.g., rodents: Gubernick and Alberts 1987; Solomon and Getz 1997; chiroptera: O’Farrell and Studier 1973; canids: Moehlman and Hofer 1997; cetaceans: Gero et al. 2009; and primates: Hrdy 1976; Chism 2000). Allomaternal care includes infant care provided by the father (paternal care, Fernandez-Duque et al. 2009) or by conspecifics other than the parents (alloparental care, Wilson 1975). While well represented by a diversity of taxa, allomaternal care is not common among mammals (e.g., 9–10% of taxa display paternal care; Kleiman and Malcolm 1981; Huck and Fernandez-Duque 2012), allomaternal care has been recently noted to occur at relatively high frequencies in the Order Primates, particularly among many haplorhine (e.g., monkey and ape) species (Tardif 1997; Chism 2000; Ross and MacLarnon 2000; Hrdy 2009). While studies have examined the causes and consequences of allomaternal care among haplorhines, to our knowledge, there has yet to be a comprehensive analysis of allomaternal care across the entire primate order (e.g., including the primates of Madagascar, hereafter referred to as lemurs). This is in large part because studies of lemur allomaternal care have lagged behind those of their primate cousins. The most recent attempt at a synthesis of primate allomaternal care found that it was a haplorhine-biased phenomenon, finding no evidence of lemurs participating in allomaternal care-related behaviors (Ross 2003), and thus precluding any analysis of allomaternal care within that taxon. However, recent increases in attention to and sampling effort of lemur care behaviors have revealed that allomaternal care is more common in lemurs than originally thought (Mitchell 1969; Klopfer 1974; Pereira et al. 1987; Wright 1990; Patel 2007; Hrdy 2010; Rowe and Myers 2011; Tecot and Hrdy, unpublished data). Moreover, a number of studies in recent years have added to our understanding of this postnatal care strategy in lemurs, making it possible to include these species in broader taxonomic comparisons of primate reproductive strategies. In light of these recent discoveries, we aim to (1) describe the different types of allomaternal care observed in primates, including a discussion of how each type of care is expressed in monkeys and apes, and a summary of what is currently known for lemurs; (2) discuss the benefits of allomaternal caretaking and whether such behaviors benefit lemur mothers; and (3) outline important gaps in our knowledge of lemur allomaternal care, suggesting future avenues of research.

Species-level view of population structure and gene flow for a critically endangered primate (Varecia variegata)

Lemurs are among the worlds most threatened mammals. The critically endangered black-and-white ruffed lemur (Varecia variegata), in particular, has recently experienced rapid population declines due to habitat loss, ecological sensitivities to habitat degradation, and extensive human hunting pressure. Despite this, a recent study indicates that ruffed lemurs retain among the highest levels of genetic diversity for primates. Identifying how this diversity is apportioned and whether gene flow is maintained among remnant populations will help to diagnose and target conservation priorities. We sampled 209 individuals from 19 sites throughout the remaining V. variegata range. We used 10 polymorphic microsatellite loci and ∼550 bp of mtDNA sequence data to evaluate genetic structure and population dynamics, including dispersal patterns and recent population declines. Bayesian cluster analyses identified two distinct genetic clusters, which optimally partitioned data into populations occurring on either side of the Mangoro River. Localities north of the Mangoro were characterized by greater genetic diversity, greater gene flow (lower genetic differentiation) and higher mtDNA haplotype and nucleotide diversity than those in the south. Despite this, genetic differentiation across all sites was high, as indicated by high average FST (0.247) and ΦST (0.544), and followed a pattern of isolation-by-distance. We use these results to suggest future conservation strategies that include an effort to maintain genetic diversity in the north and restore connectivity in the south. We also note the discordance between patterns of genetic differentiation and current subspecies taxonomy, and encourage a re-evaluation of conservation management units moving forward.

What drives flexibility in primate social organization

The importance of behavioral flexibility for understanding primate ecology and evolutionary diversity is becoming increasingly apparent, and yet despite the abundance of long-term studies across diverse sampling localities, we still do not understand the myriad factors responsible for among-site variation in species’ social organization. The goals of our study were to address this question via three main objectives: to quantify social organization flexibility (i.e., across-site intraspecific variation) of well-studied primate species, test the idea that closely related species exhibit similar levels of flexibility, and test hypotheses explaining variation in social organization flexibility among primate species. We obtained data for a total of 175 study sites from 32 primate species representing all major primate clades. We employed phylogenetic principal components analysis to quantify social organization flexibility for each species. We quantified the phylogenetic signal in social organization flexibility and then evaluated the best predictors of flexibility. We found that mean group size was positively related to social organization flexibility. Large social groups may be more flexible because the foraging costs and predation risk associated with adding or subtracting individuals are lower compared to small social groups. There was some support that absolute brain size and the presence of fission–fusion dynamics were also related to high levels of social organization flexibility, suggesting that cognitive ability and/or within-site behavioral flexibility may also lead to increased variation across sites. Our results serve as an early step in understanding the patterns and processes related to social organization flexibility in primates and other social mammals.

Morphometrics of wild black‐and‐white ruffed lemurs [Varecia variegata; Kerr, 1792]

This study presents the first detailed morphometric measurements of wild caught black‐and‐white ruffed lemurs (Varecia variegata) from the eastern rainforests of Madagascar and aims to quantify the morphological variation present throughout their recognized range. One hundred and forty‐four adult and juvenile individuals from 15 sites were sampled for 20 cranial, dental and postcranial morphometric and body mass measurements. Data were collected from an equal number of male and female individuals sampled across seasons over a 7‐year period (1999–2002, 2004–2006). Results indicate that adult body mass and morphometric measurements varied between sexes across sites; however, the only significant intersexual difference found was that females possessed, on average, longer tails than males. Contrary to previous studies, significant seasonal variation could not be detected in either male or female body mass or testicular volume (i.e., breeding vs. nonbreeding, food‐scarce vs. food‐abundant seasons). Measurements did, however, vary significantly by site and subspecies, though clinal variation could not explain these differences. The introduced population from Nosy Mangabe exhibited significantly lower body mass and overall body length than all other populations; however, this distinction may not have been attributable to natural variation, and may have instead resulted from the ecologically restrictive habitat (e.g., unusually high lemur population densities, limited food resources, ecological isolation) of this introduced population. Finally, although fore‐to‐hindlimb, brachium‐to‐thigh and hindlimb indices were comparable to previous values, forelimb indices calculated here deviate significantly from previous reports, placing V. variegata within the upper range of lemurid taxa. It is currently unknown whether this is an artifact of sampling methods (i.e., live vs. skeletal specimens) or whether this is an avenue that warrants further investigation. Am. J. Primatol. 70:913–926, 2008.

Profiling caregivers: Hormonal variation underlying allomaternal care in wild red-bellied lemurs, Eulemur rubriventer

Neuroendocrine evidence suggests that paternal care is mediated by hormonal mechanisms, where hormonal changes in expectant and new fathers facilitate infant care. In species with obligate and extensive paternal care such as humans, androgen levels decline once males are paired and have offspring, and in direct response to offspring care. Facultative infant care is widespread in the Order Primates, but the underlying hormonal mechanisms are largely unknown. We found that wild, red-bellied lemurs living in family groups (two adults and their presumed offspring) varied in the amount of care they provided infants. The more fathers invested in helping infants (measured as a composite of carrying, holding, huddling, grooming, and playing), and specifically the more they huddled and groomed with infants, the higher their fecal androgen (fA) levels, contrary to expectations. Carrying was negatively related to fA levels. Helping by subadults and juveniles was not related to their own fA levels. Elevated fA levels during infant dependence have been observed in other vertebrate species, and are thought to reflect reinvestment in mating rather than investment in dependent offspring. However, red-bellied lemurs do not mate until after infants are weaned, and they have long-term pair-bonds, suggesting that elevated fA levels play a role in offspring care. These results support a growing body of research suggesting that elevated androgen levels do not inhibit protective infant care.

Social behaviour and gut microbiota in red‐bellied lemurs (Eulemur rubriventer): In search of the role of immunity in the evolution of sociality

Vertebrate gut microbiota form a key component of immunity and a dynamic link between an individual and the ecosystem. Microbiota might play a role in social systems as well, because microbes are transmitted during social contact and can affect host behaviour. Combining methods from behavioural and molecular research, we describe the relationship between social dynamics and gut microbiota of a group-living cooperative species of primate, the red-bellied lemur (Eulemur rubriventer). Specifically, we ask whether patterns of social contact (group membership, group size, position in social network, individual sociality) are associated with patterns of gut microbial composition (diversity and similarity) between individuals and across time. Red-bellied lemurs were found to have gut microbiota with slight temporal fluctuations and strong social group-specific composition. Contrary to expectations, individual sociality was negatively associated with gut microbial diversity. However, position within the social network predicted gut microbial composition. These results emphasize the role of the social environment in determining the microbiota of adult animals. Since social transmission of gut microbiota has the potential to enhance immunity, microbiota might have played an escalating role in the evolution of sociality.