Richard R. Lawler

Beza Mahafaly Special Reserve: Long-Term Research on Lemurs in Southwestern Madagascar

The Beza Mahafaly Project in southwestern Madagascar was founded in 1975. It was established as a collaborative effort among the University of Madagascar (now University of Antananarivo), Washington University, Yale University, and the local communities for long-term training and research, biodiversity conservation, and socioeconomic development. Beza Mahafaly consists of two noncontiguous forest parcels separated by 10 km that became a protected area (Reserve Speciale) in 1986: an 80-ha gallery forest and a 520-ha xerophytic spiny forest. The region has a diversity of habitats and a very diverse and highly endemic flora and fauna, including four species of lemurs found in or near the reserve. The ringtailed lemur (Lemur catta) and Verreaux’s sifaka (Propithecus verreauxi) have been the subject of our long-term research. In this chapter we highlight some of the results of this research. Our multidisciplinary studies illustrate the feasibility of collecting long-term data on careers of individual animals and of obtaining large samples on numerous animals, across numerous social groups, in relatively isolated breeding populations. Thus, we can provide insights into many of the demographic, socioecological, anthropogenic, and epidemiological factors that shape the local ringtailed lemur and sifaka population. Here we summarize how ringtailed lemur demographic structure is affected by climatic perturbations (drought); how aspects of general health (parasite loads and dental health) are directly related to habitat, dietary, and anthropogenic factors; how tight birth seasonality in sifaka can elicit stress responses in males associated with increased male aggression, group takeovers, and infanticide risk; how life history schedules are related to evolutionary responses to extreme climatic fluctuations; and how directional selection among sifaka males leads to longer, stronger legs, but not to increase in male body mass relative to females.

Morphological integration and natural selection in the postcranium of wild verreaux's sifaka (Propithecus verreauxi verreauxi)

Morphological integration manifests as strong phenotypic covariation among interacting traits. In this study, a graph-theory approach is used to analyze patterns of morphological integration in a wild population of Verreauxs sifaka (Propithecus verreauxi verreauxi). The motivation for this study is to determine the relative roles of development versus function in shaping patterns of morphological integration in the sifaka postcranium. A developmental and a functional hypothesis of integration are compared with the observed pattern of integration and the fit of these hypotheses is assessed using information theoretic statistics. Correlational selection is also estimated on limb elements. Information theoretic statistics indicate that the developmental hypothesis fits the observed pattern of integration slightly better than the functional hypothesis. Only two pairs of traits experience correlational selection but neither of the traits within each pair are morphologically integrated. The observed pattern of integration contains several trait-trait associations that are specified by both the functional and developmental hypotheses. These results likely reflect the nested covariation structure in which a novel locomotor mode, vertical clinging and leaping, is derived from a primitive quadrupedal morphotype.

Linking genotypes, phenotypes, and fitness in wild primate populations

In the decade since the first draft of the human genome was announced, 1 genome sequencing projects have been initiated for an additional twenty‐some primate species. Within the next several years, genome sequence data will likely become available for all primate genera and for most individuals within some primate populations. 2 , 3 At the same time, gene mapping and association studies of humans and other organisms are rapidly advancing our understanding of the genetic bases of behavioral and morphological traits. Primatologists are especially well‐placed to take advantage of this coming flood of genetic data. Here we discuss what this new era of primate genomics means for field primatology and highlight some of the unprecedented opportunities it will afford, particularly with regard to examining the genetic basis of primate adaptation and diversity.

Evaluating ring-tailed lemurs (Lemur catta) from southwestern Madagascar for a genetic population bottleneck

In light of historical and recent anthropogenic influences on Malagasy primate populations, in this study ring-tailed lemur (Lemur catta) samples from two sites in southwestern Madagascar, Beza Mahafaly Special Reserve (BMSR) and Tsimanampetsotsa National Park (TNP), were evaluated for the genetic signature of a population bottleneck. A total of 45 individuals (20 from BMSR and 25 from TNP) were genotyped at seven microsatellite loci. Three methods were used to evaluate these populations for evidence of a historical bottleneck: M-ratio, mode-shift, and heterozygosity excess tests. Three mutation models were used for heterozygosity excess tests: the stepwise mutation model (SMM), two-phase model (TPM), and infinite allele model (IAM). M-ratio estimations indicated a potential bottleneck in both populations under some conditions. Although mode-shift tests did not strongly indicate a population bottleneck in the recent historical past when samples from all individuals were included, a female-only analysis indicated a potential bottleneck in TNP. Heterozygosity excess was indicated under two of the three mutation models (IAM and TPM), with TNP showing stronger evidence of heterozygosity excess than BMSR. Taken together, these results suggest that a bottleneck may have occurred among L. catta in southwestern Madagascar in the recent past. Given knowledge of how current major stochastic climatic events and human-induced change can negatively impact extant lemur populations, it is reasonable that comparable events in the historical past could have caused a population bottleneck. This evaluation additionally functions to highlight the continuing environmental and anthropogenic challenges faced by lemurs in southwestern Madagascar.

Novel opsin gene variation in large-bodied, diurnal lemurs

Some primate populations include both trichromatic and dichromatic (red–green colour blind) individuals due to allelic variation at the X-linked opsin locus. This polymorphic trichromacy is well described in day-active New World monkeys. Less is known about colour vision in Malagasy lemurs, but, unlike New World monkeys, only some day-active lemurs are polymorphic, while others are dichromatic. The evolutionary pressures underlying these differences in lemurs are unknown, but aspects of species ecology, including variation in activity pattern, are hypothesized to play a role. Limited data on X-linked opsin variation in lemurs make such hypotheses difficult to evaluate. We provide the first detailed examination of X-linked opsin variation across a lemur clade (Indriidae). We sequenced the X-linked opsin in the most strictly diurnal and largest extant lemur, Indri indri, and nine species of smaller, generally diurnal indriids (Propithecus). Although nocturnal Avahi (sister taxon to Propithecus) lacks a polymorphism, at least eight species of diurnal indriids have two or more X-linked opsin alleles. Four rainforest-living taxa—I. indri and the three largest Propithecus species—have alleles not previously documented in lemurs. Moreover, we identified at least three opsin alleles in Indri with peak spectral sensitivities similar to some New World monkeys.

The Locomotor Behavior of Callicebus brunneus and Callicebus torquatus

This study presents data on the positional behavior of Callicebus torquatus and Callicebus brunneus collected from two different localities in Peru. C. brunneus primarily utilizes short-distance, bounding leaps, while C. torquatus relies predominantly on quadrupedal walking. Both species utilize small, horizontal and terminal branches more than any other substrate class. We relate the differences in locomotor behaviors between the two species to their utilization of different forest levels. C. brunneus tends to reside in the understory and brush layer forest levels. These more discontinuous strata necessitate higher frequencies of short-distance leaping. C. torquatus occupies the more continuous, interconnected canopy level, and much of its food is found in this level. Comparisons with other species show that Callicebus spp. locomote along smaller-sized, horizontal branches using quadrupedal progression and leaping.

Monomorphism, male-male competition, and mechanisms of sexual dimorphism.

Reconstructing sociosexual variables such as mating system and social organization from fragmentary fossils and other sources of data remains a major challenge in understanding the evolution of behavioral and morphological diversity within the primate order. Often, a particular mating system can lead to the evolution of novel behavior (e.g., ‘‘competitive’’ paternal care in tamarins; Garber, 1997) or contribute to the evolution of a particular morphology (e.g., relatively larger sagittal crests in male gorillas with large harems; Caillaud et al., 2008). Indeed, within paleoanthropology, numerous hypotheses concerning the evolution of major adaptive traits in humansdbipedalism, language, increased reliance on stone tool-usedoften rely on a particular inferred mating system. For example, Lovejoy (1981) proposed that monogamy was the ancestral mating system in Australopithecus afarensis and from this went on to craft a creative hypothesis for the evolution of bipedalism. Similarly, Deacon (1997) suggested that male-female pairbonding helped foster the evolution of language by allowing males and females to vocalize their monogamous commitment to other group members. Increased reliance on stone tools has also been linked to a particular mating system and social organization, with a concomitant reduction in canine size (e.g., Wolpoff, 1976). These examples, and others like them, suggest particular sociosexual behaviors and mating systems were a potential driver of the evolution of unique human characteristics within the order Primates. It is not surprising, then, that any hypothesized mating system inferred from fragmentary fossil data is likely to draw scrutiny; this has particularly been the case for hypotheses

Demographic concepts and research pertaining to the study of wild primate populations

Demography is the study of individuals as members of a population. The dynamics of a population are determined by collectively analyzing individual schedules of survival, growth, and reproduction. Together, these schedules are known as the vital rates of the population. The vital rates, along with dispersal, contribute to population structure, which refers to how the population is organized by age, sex, density, and social groups. I briefly review the history of anthropological demography as it pertains to wild primates and then I discuss basic demographic concepts and approaches for studying wild primate populations. I then turn to demographic studies of wild primate demography. Primates are generally characterized by high adult survival probabilities relative to survival at other age/stage classes and most primate populations have population growth rates near equilibrium. Changes in adult survival have the greatest impact on population growth rate (i.e., fitness) relative to other demographic traits such as juvenile/yearling survival or age at first reproduction. I discuss how these demographic patterns, and others, connect to topics and issues in behavioral ecology, life history theory, population genetics, and conservation biology. These connections help reaffirm the fact that the vital rates are both targets and agents of evolutionary change. In this regard, demographic studies of wild primates provide a critical link between the proximate socioecological processes that operate in a species and the long-term phylogenetic patterns that characterize a species.

Testing for a Historical Population Bottleneck in Wild Verreaux's Sifaka (Propithecus verreauxi verreauxi) Using Microsatellite Data

The degree to which historical human activities negatively impacted past and present lemur species is a long‐standing question in primatology. At present, most evidence addressing this issue comes from archaeology, paleontology, and behavioral studies. Genetic data provide another source of evidence. In this study, six microsatellite loci, genotyped on more than 360 wild Verreauxs sifaka, are used in order to test the hypothesis that this population experienced a population bottleneck in the last 2000 years. Excess heterozygosity is compared with the heterozygosity expected under mutation‐drift equilibrium in order to test for the genetic signature of a rapid population contraction in the past. The results indicate that the sifaka population did not experience a population bottleneck. Various methodological and conceptual implications of this result are discussed. Am. J. Primatol. 70:990–994, 2008.

Long-term field studies of lemurs, lorises, and tarsiers

Lemurs, lorises, and tarsiers are socially and ecologically diverse primates that include some of the most endangered mammals. We review results of long-term studies of 15 lemur species from 7 sites in Madagascar and 1 species each of loris and tarsier in Indonesia. We emphasize that the existence of long-term study populations is a crucial prerequisite for planning and conducting shorter studies on specific topics, as exemplified by various ecophysiological studies of lemurs. Extended studies of known individuals have revealed variation in social organization within and between ecologically similar species. Even for these primates with relatively fast life histories, it required more than a decade of paternity data to characterize male reproductive skew. The long-term consequences of female rank on reproductive success remain poorly known, however. Long-term monitoring of known individuals is the only method to obtain data on life-history adaptations, which appear to be shaped by predation in the species covered here; long-term studies are also needed for addressing particular questions in community ecology. The mere presence of long-term projects has a positive effect on the protection of study sites, and they generate unique data that are fundamental to conservation measures, such as close monitoring of populations.