Rachel L. Jacobs

The Crisis of the Critically Endangered Greater Bamboo Lemur (Prolemur simus)

Abstract: Prolemur simus (the greater bamboo lemur) is the most abundant lemur in the northern subfossil sites of Madagascar. Living populations still persist, but in low numbers within a diminished range, making it one of the most critically endangered lemurs. Over the past twenty years scientists have searched the south- and central-eastern rain forests of Madagascar. Despite surveys that encompass over 500 km2, less than 75 animals have been found, with a recent total count of 60. More encouraging is that in 2007 two new sites containing P. simus were found: Mahasoa an unprotected 150 ha fragment east of the Ranomafana/Andringitra corridor (17 P. simus), and Torotorofotsy, a RAMSAR site near Andasibe (∼16 P. simus). Prolemur simus is a bamboo specialist with a patchy geographic distribution, which may be driven by the distribution of one or two bamboo species. Home ranges are large, group size has been observed to be from four to 26 individuals, and localities may be spaced hundreds of kilometers apart. Ranomafana National Park contains the only fully habituated group, and there are a total of three groups known in the park. We make recommendations for conservation action for these populations of P. simus. If immediate action is taken, we may be able to prevent the extinction of this species within the next decades.

Comparative functional morphology of the primate peroneal process

The first metatarsal of living Primates is characterized by a well-developed peroneal process, which appears proportionally larger in prosimians than in anthropoids. A large peroneal process has been hypothesized to: 1) reflect powerful hallucal grasping, 2) act as a buttress to reduce strain from loads acting on the entocuneiform-first metatarsal joint during landing and grasping after a leap, and/or 3) correlate with differences in physiological abduction of the hallux. In this study, we address the latter two hypotheses by comparing the morphology of the peroneal process in 143 specimens representing 37 species of extant prosimians, platyrrhine anthropoids, and tupaiids (tree shrews) that engage in different locomotor behaviors. In particular, we compare taxa that vary in leaping frequency and hallucal abduction. Linear and angular measurements on the first metatarsal were obtained to evaluate differences in relative peroneal process thickness and length, first metatarsal abduction angle, and overall first metatarsal shape. Leaping frequency was significantly correlated only with relative peroneal process thickness within extant lorisoids. Relative process length was positively correlated with the angle of hallucal abduction within prosimians; this angle is significantly greater in prosimians than anthropoids. Multivariate analyses of metatarsal shape effectively separate species along phylogenetic lines, but not by locomotor behaviors. The hypothesis that the peroneal process on the first metatarsal reduces the loads on the entocuneiform-first metatarsal joint during landing after a leap is in part supported by data from extant lorisoids (i.e., slow quadrupedal lorises vs. leaping galagos). A peroneal process of greater length within prosimians may serve to increase the lever arm for the peroneus longus muscle in order to prevent hyper-abduction, followed by inversion in locomotor situations where the animals weight is born on a highly divergent/abducted hallux.

Opsin Genes and Visual Ecology in a Nocturnal Folivorous Lemur

Primate color vision has traditionally been examined in the context of diurnal activity, but recent genetic and ecological studies suggest that color vision plays a role in nocturnal primate behavior and ecology as well. In this study, we united molecular analyses of cone visual pigment (opsin) genes with visual modeling analyses of food items to explore the evolution of color vision in the folivorous woolly lemur (genus Avahi). Previous studies have shown that leaf quality, e.g., protein content, leaf toughness, and protein/toughness ratio, is significantly correlated with green-red and blue-yellow chromatic differences, suggesting a potential role of color in leaf discrimination in Avahi, and, consequently, a potential adaptive advantage to color vision in this taxon. Phylogenetic selection tests determined that the strength of selection on the SWS1 opsin gene to retain blue-sensitive SWS cones did not significantly differ in Avahi compared to day-active primates. Genotyping of the M/LWS opsin gene in 60 individuals from nine species found that the 558-nm-sensitive (red-sensitive) allele is conserved across all Avahi. Finally, we measured spectral reflectance from five species of young leaves consumed by Avahi and background foliage in Ranomafana National Park and modeled performance of possible S and M/L pigment pairs for detecting these food items under different nocturnal illuminations (e.g. twilight, moonlight). We found that the observed cone pigment pair in Avahi was optimally tuned for color-based detection of young green leaves in all nocturnal light environments, suggesting a potential adaptive role of nocturnal color vision in selection for dichromacy in this genus.

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.

Considering the Influence of Nonadaptive Evolution on Primate Color Vision.

Color vision in primates is variable across species, and it represents a rare trait in which the genetic mechanisms underlying phenotypic variation are fairly well-understood. Research on primate color vision has largely focused on adaptive explanations for observed variation, but it remains unclear why some species have trichromatic or polymorphic color vision while others are red-green color blind. Lemurs, in particular, are highly variable. While some species are polymorphic, many closely-related species are strictly dichromatic. We provide the first characterization of color vision in a wild population of red-bellied lemurs (Eulemur rubriventer, Ranomafana National Park, Madagascar) with a sample size (87 individuals; NX chromosomes = 134) large enough to detect even rare variants (0.95 probability of detection at ≥ 3% frequency). By sequencing exon 5 of the X-linked opsin gene we identified opsin spectral sensitivity based on known diagnostic sites and found this population to be dichromatic and monomorphic for a long wavelength allele. Apparent fixation of this long allele is in contrast to previously published accounts of Eulemur species, which exhibit either polymorphic color vision or only the medium wavelength opsin. This unexpected result may represent loss of color vision variation, which could occur through selective processes and/or genetic drift (e.g., genetic bottleneck). To indirectly assess the latter scenario, we genotyped 55 adult red-bellied lemurs at seven variable microsatellite loci and used heterozygosity excess and M-ratio tests to assess if this population may have experienced a recent genetic bottleneck. Results of heterozygosity excess but not M-ratio tests suggest a bottleneck might have occurred in this red-bellied lemur population. Therefore, while selection may also play a role, the unique color vision observed in this population might have been influenced by a recent genetic bottleneck. These results emphasize the need to consider adaptive and nonadaptive mechanisms of color vision evolution in primates.

Primate genotyping via high resolution melt analysis: rapid and reliable identification of color vision status in wild lemurs

Analyses of genetic polymorphisms can aid our understanding of intra- and interspecific variation in primate sociality, ecology, and behavior. Studies of primate opsin genes are prime examples of this, as single nucleotide variants (SNVs) in the X-linked opsin gene underlie variation in color vision. For primate species with polymorphic trichromacy, genotyping opsin SNVs can generally indicate whether individual primates are red-green color-blind (denoted homozygous M or homozygous L) or have full trichromatic color vision (heterozygous ML). Given the potential influence of color vision on behavior and fitness, characterizing the color vision status of study subjects is becoming commonplace for many primate field projects. Such studies traditionally involve a multi-step sequencing-based method that can be costly and time-consuming. Here we present a new reliable, rapid, and relatively inexpensive method for characterizing color vision in primate populations using high resolution melt analysis (HRMA). Using lemurs as a case study, we characterized variation at exons 3 and/or 5 of the X-linked opsin gene for 87 individuals representing nine species. We scored opsin genotypes and color vision status using both traditional sequencing-based methods as well as our novel melting-curve based HRMA protocol. For each species, the melting curves of varying genotypes (homozygous M, homozygous L, heterozygous ML) differed in melting temperature and/or shape. Melting curves for each sample were consistent across replicates, and genotype-specific melting curves were consistent across DNA sources (blood vs. feces). We show that opsin genotypes can be quickly and reliably scored using HRMA once lab-specific reference curves have been developed based on known genotypes. Although the protocol presented here focuses on genotyping lemur opsin loci, we also consider the larger potential for applying this approach to various types of genetic studies of primate populations.

Parentage complexity in socially monogamous lemurs (Eulemur rubriventer): Integrating genetic and observational data

Genetic analyses of parentage sometimes reveal that “socially monogamous” (pair‐living) species do not reside in strict family groups. Circumstances such as adult turnovers and extra‐pair copulations, among others, may result in non‐nuclear families. These genetic relationships within groups have implications for interpreting social behaviors. Red‐bellied lemurs (Eulemur rubriventer) live in groups generally comprising an adult male‐female pair plus immatures, and early genetic analyses of parentage in a relatively small sample suggested they mate monogamously. However, previous research on this taxon has also identified scenarios in which non‐nuclear families might result, such as adult turnovers. To assess the potential occurrence of non‐nuclear families in this “socially monogamous” taxon, as well as the social conditions under which they might occur, we combined behavioral observations of wild red‐bellied lemurs in Ranomafana National Park with genetic parentage analysis of immatures from 17 groups. We found that the majority of groups (75%) represented nuclear family groups. However, 25% of groups represented non‐nuclear families at some point during the study. The social factors that resulted in non‐nuclear families were varied and included at least one adult turnover, and potentially delayed female dispersals and extra‐pair copulations. Our results suggest that red‐bellied lemurs are generally reproductively monogamous, with only limited evidence that non‐nuclear families result from non‐monogamous reproduction. However, similar to other pair‐living primates, red‐bellied lemurs appear to exhibit flexibility in their social organization and mating strategies. Multiple lines of evidence should be considered when inferring parent‐offspring relationships within pair‐living groups.

Celebrating fifty years of research at the Duke Lemur Center

This year marked the 50 anniversary of the Duke Lemur Center (DLC). Founded in 1966 by John Buettner-Janusch and Peter Klopfer, the DLC is currently home to more than 200 lemurs and, over the years, has become one of the world’s most renowned centers for lemur research. The DLC’s birthday bash was held in Durham, NC from September 21 through 23, 2016 The event was first and foremost a celebration of the DLC’s impact on lemur research, drawing a crowd of lemur scientists and enthusiasts from around the globe. Wednesday night’s opening reception kicked off with a welcome from the current DLC Director, Anne Yoder, and remarks from co-founder Peter Klopfer. The following twoday scientific symposium featured podium presentations on Thursday and Friday at the Duke Washington Inn and Golf Club. A poster session was held Thursday evening at the DLC, providing a welcome opportunity, despite the rain, for attendees to tour the recently renovated facilities. The symposium showcased research on cognition and behavior, physiology and aging, and conservation and health. Videos of all research presentations are available on the DLC’s YouTube channel.

The gateway to anthropology in st. Louis

T his year, St. Louis, Missouri, was host to the annual meeting of the American Association of Physical Anthropologists (AAPA), which took place March 25–28, 2015. More than 1,000 anthropologists from across the world met near St. Louis’s Gateway Arch, where exciting presentations covered a diverse array of topics, from genetics in Neanderthals to energetics in humans. New research explored physiology and competition in primatology and postcranial adaptations in functional morphology. Highlights also included the presentation of new fossils that promise to influence our current understanding of human evolution.

Inaugural meeting of the Northeastern Evolutionary Primatologists group.

R utgers University was host to the inaugural meeting of the Northeastern Evolutionary Primatologists (NEEP) group on November 7–8 2014. Ryne Palombit and Erin Vogel of Rutgers and Andreas Koenig and Carola Borries of Stony Brook organized the conference. At a general meeting, conference participants discussed the naming of the group and its constitution and bylaws. The group’s temporary name was officially changed and NEEP officials were also elected, with Ryne Palombit now serving as president and Andreas Koenig as president-elect. Other positions were also filled, including secretary (Andrea Baden, Hunter), treasurer (Carola Borries), student liaison (Emma Cancelliere, Hunter College), and web master (Megan Petersdorf, NYU). Those interested in being added to the NEEP email list should contact Carola Borries at <ne.evol.primatol@gmail.com>. The conference began with a keynote address by Jenny Tung (Duke). Using three examples from her ongoing research, she discussed “How the social environment shapes the genome: lessons from functional genomic studies of baboons and rhesus macaques.” Experimental manipulation of dominance ranks among female rhesus macaques identified social status as a primary predictor of variation in levels of gene expression, particularly those involved in immune surveillance and defense. Variation in gene expression could be used to predict rank class with 80% accuracy. By applying her methods to wild primate populations (here, yellow baboons of Amboseli), Tung has assessed differences in DNA methylation in wild-feeding versus food-enhanced groups. Results suggest that available resources influence the resulting DNA methylation patterns and highlight the importance of enhancer elements in the baboon genome. Tung’s presentation wrapped up with a discussion of gut microbiome variation. Frequent grooming partners share more similar gut microbiomes. Her work demonstrated how social networks mediate differences in gut microbiome composition across social groups. Saturday, kicked off with a session on life history, development, and speciation. This first of three sessions focused on reproductive aging in orangutans (Lara Durgavitch, Harvard), the use of trace element analyses to identify variation in primate weaning (Tanya Smith, Harvard), and the application of ecological niche models to understand primate niche divergence and speciation (Mary Blair, AMNH). Caitlin O’Connell (Boston University) reported that adolescent orangutan females, in contrast to adults in Gunung Palung, Borneo, are highly social. They even engage in long bouts of sexual behavior with flanged males, suggesting that adolescence is an important period for female social development in orangutans. Nicole Thompson (Columbia) examined how social behavior and demographic parameters influence survival in female blue monkeys. Her research indicates that grooming behavior, particularly