Publications by authors named "Richard R Lawler"

27 Publications

  • Page 1 of 1

The long lives of primates and the 'invariant rate of ageing' hypothesis.

Nat Commun 2021 06 16;12(1):3666. Epub 2021 Jun 16.

Dian Fossey Gorilla Fund International, Atlanta, GA, USA.

Is it possible to slow the rate of ageing, or do biological constraints limit its plasticity? We test the 'invariant rate of ageing' hypothesis, which posits that the rate of ageing is relatively fixed within species, with a collection of 39 human and nonhuman primate datasets across seven genera. We first recapitulate, in nonhuman primates, the highly regular relationship between life expectancy and lifespan equality seen in humans. We next demonstrate that variation in the rate of ageing within genera is orders of magnitude smaller than variation in pre-adult and age-independent mortality. Finally, we demonstrate that changes in the rate of ageing, but not other mortality parameters, produce striking, species-atypical changes in mortality patterns. Our results support the invariant rate of ageing hypothesis, implying biological constraints on how much the human rate of ageing can be slowed.
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http://dx.doi.org/10.1038/s41467-021-23894-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8209124PMC
June 2021

Comparative genomic analysis of sifakas () reveals selection for folivory and high heterozygosity despite endangered status.

Sci Adv 2021 Apr 23;7(17). Epub 2021 Apr 23.

Human Genome Sequencing Center and Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 77030, USA.

Sifakas (genus ) are critically endangered, large-bodied diurnal lemurs that eat leaf-based diets and show corresponding anatomical and microbial adaptations to folivory. We report on the genome assembly of Coquerel's sifaka () and the resequenced genomes of Verreaux's (), the golden-crowned (), and the diademed () sifakas. We find high heterozygosity in all sifakas compared with other primates and endangered mammals. Demographic reconstructions nevertheless suggest declines in effective population size beginning before human arrival on Madagascar. Comparative genomic analyses indicate pervasive accelerated evolution in the ancestral sifaka lineage affecting genes in several complementary pathways relevant to folivory, including nutrient absorption and xenobiotic and fatty acid metabolism. Sifakas show convergent evolution at the level of the pathway, gene family, gene, and amino acid substitution with other folivores. Although sifakas have relatively generalized diets, the physiological challenges of habitual folivory likely led to strong selection.
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http://dx.doi.org/10.1126/sciadv.abd2274DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8064638PMC
April 2021

Maternal death and offspring fitness in multiple wild primates.

Proc Natl Acad Sci U S A 2021 01;118(1)

Department of Biology, Duke University, Durham, NC 27708;

Primate offspring often depend on their mothers well beyond the age of weaning, and offspring that experience maternal death in early life can suffer substantial reductions in fitness across the life span. Here, we leverage data from eight wild primate populations (seven species) to examine two underappreciated pathways linking early maternal death and offspring fitness that are distinct from direct effects of orphaning on offspring survival. First, we show that, for five of the seven species, offspring face reduced survival during the years immediately preceding maternal death, while the mother is still alive. Second, we identify an intergenerational effect of early maternal loss in three species (muriquis, baboons, and blue monkeys), such that early maternal death experienced in one generation leads to reduced offspring survival in the next. Our results have important implications for the evolution of slow life histories in primates, as they suggest that maternal condition and survival are more important for offspring fitness than previously realized.
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http://dx.doi.org/10.1073/pnas.2015317118DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7821045PMC
January 2021

Age-associated epigenetic change in chimpanzees and humans.

Philos Trans R Soc Lond B Biol Sci 2020 11 21;375(1811):20190616. Epub 2020 Sep 21.

Center for the Advanced Study of Human Paleobiology, Department of Anthropology, The George Washington University, Washington, DC 20052, USA.

Methylation levels have been shown to change with age at sites across the human genome. Change at some of these sites is so consistent across individuals that it can be used as an 'epigenetic clock' to predict an individual's chronological age to within a few years. Here, we examined how the pattern of epigenetic ageing in chimpanzees compares with humans. We profiled genome-wide blood methylation levels by microarray for 113 samples from 83 chimpanzees aged 1-58 years (26 chimpanzees were sampled at multiple ages during their lifespan). Many sites (greater than 65 000) showed significant change in methylation with age and around one-third (32%) of these overlap with sites showing significant age-related change in humans. At over 80% of sites showing age-related change in both species, chimpanzees displayed a significantly faster rate of age-related change in methylation than humans. We also built a chimpanzee-specific epigenetic clock that predicted age in our test dataset with a median absolute deviation from known age of only 2.4 years. However, our chimpanzee clock showed little overlap with previously constructed human clocks. Methylation at CpGs comprising our chimpanzee clock showed moderate heritability. Although the use of a human microarray for profiling chimpanzees biases our results towards regions with shared genomic sequence between the species, nevertheless, our results indicate that there is considerable conservation in epigenetic ageing between chimpanzees and humans, but also substantial divergence in both rate and genomic distribution of ageing-associated sites. This article is part of the theme issue 'Evolution of the primate ageing process'.
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http://dx.doi.org/10.1098/rstb.2019.0616DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7540949PMC
November 2020

Genetic population structure of endangered ring-tailed lemurs () from nine sites in southern Madagascar.

Ecol Evol 2020 Aug 16;10(15):8030-8043. Epub 2020 Jul 16.

Department of Anthropology Hunter College of the City University of New York New York NY USA.

Madagascar's ring-tailed lemurs () are experiencing rapid population declines due to ongoing habitat loss and fragmentation, as well as increasing exploitation for bushmeat and the illegal pet trade. Despite being the focus of extensive and ongoing behavioral studies, there is comparatively little known about the genetic population structuring of the species. Here, we present the most comprehensive population genetic analysis of ring-tailed lemurs to date from across their likely remaining geographic range. We assessed levels of genetic diversity and population genetic structure using multilocus genotypes for 106 adult individuals from nine geographically representative localities. Population structure and analyses revealed moderate genetic differentiation with localities being geographically partitioned into northern, southern, western and also potentially central clusters. Overall genetic diversity, in terms of allelic richness and observed heterozygosity, was high in the species (AR = 4.74,  = 0.811). In fact, it is the highest among all published lemur estimates to date. While these results are encouraging, ring-tailed lemurs are currently affected by ongoing habitat fragmentation and occur at lower densities in poorer quality habitats. The effects of continued isolation and fragmentation, coupled with climate-driven environmental instability, will therefore likely impede the long-term viability of the species.
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http://dx.doi.org/10.1002/ece3.6337DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7417237PMC
August 2020

Epigenetic Clocks.

Evol Anthropol 2018 Nov 1;27(6):256-260. Epub 2018 Nov 1.

Department of Sociology and Anthropology, James Madison University, Harrisonburg, Virginia.

Recent research has revealed clock-like patterns of epigenetic change across the life span in humans. Models describing these epigenetic changes have been dubbed "epigenetic clocks," and they can not only predict chronological age but also reveal biological age, which measures physiological homeostasis and deterioration over the life span. Comparative studies of the epigenetic clocks of different primate species are likely to provide insights into the evolution of life history schedules, as well as shed light on the physiological and genetic bases of aging and aging-related diseases. Chronological age estimation using clock-based calculators may also offer biological anthropologists a useful tool for applying to forensic and demographic studies.
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http://dx.doi.org/10.1002/evan.21745DOI Listing
November 2018

Novel opsin gene variation in large-bodied, diurnal lemurs.

Biol Lett 2017 Mar;13(3)

Center for the Advanced Study of Human Paleobiology, Department of Anthropology, The George Washington University, Washington, DC 20052, USA

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, , and nine species of smaller, generally diurnal indriids (). Although nocturnal (sister taxon to ) lacks a polymorphism, at least eight species of diurnal indriids have two or more X-linked opsin alleles. Four rainforest-living taxa- and the three largest species-have alleles not previously documented in lemurs. Moreover, we identified at least three opsin alleles in with peak spectral sensitivities similar to some New World monkeys.
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http://dx.doi.org/10.1098/rsbl.2017.0050DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5377041PMC
March 2017

Non-human primates avoid the detrimental effects of prenatal androgen exposure in mixed-sex litters: combined demographic, behavioral, and genetic analyses.

Am J Primatol 2016 Dec 19;78(12):1304-1315. Epub 2016 Jul 19.

Institute for Genome Sciences and Program in Personalized and Genomic Medicine, University of Maryland School of Medicine, Baltimore, Maryland.

Producing single versus multiple births has important life history trade-offs, including the potential benefits and risks of sharing a common in utero environment. Sex hormones can diffuse through amniotic fluid and fetal membranes, and females with male littermates risk exposure to high levels of fetal testosterone, which are shown to have masculinizing effects and negative fitness consequences in many mammals. Whereas most primates give birth to single offspring, several New World monkey and strepsirrhine species regularly give birth to small litters. We examined whether neonatal testosterone exposure might be detrimental to females in mixed-sex litters by compiling data from long-term breeding records for seven primate species (Saguinus oedipus; Varecia variegata, Varecia rubra, Microcebus murinis, Mirza coquereli, Cheirogaleus medius, Galago moholi). Litter sex ratios did not differ from the expected 1:2:1 (MM:MF:FF for twins) and 1:2:2:1 (MMM:MMF:MFF:FFF for triplets). Measures of reproductive success, including female survivorship, offspring-survivorship, and inter-birth interval, did not differ between females born in mixed-sex versus all-female litters, indicating that litter-producing non-human primates, unlike humans and rodents, show no signs of detrimental effects from androgen exposure in mixed sex litters. Although we found no evidence for CYP19A1 gene duplications-a hypothesized mechanism for coping with androgen exposure-aromatase protein evolution shows patterns of convergence among litter-producing taxa. That some primates have effectively found a way to circumvent a major cost of multiple births has implications for understanding variation in litter size and life history strategies across mammals.
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http://dx.doi.org/10.1002/ajp.22583DOI Listing
December 2016

Paternity in wild ring-tailed lemurs (Lemur catta): Implications for male mating strategies.

Am J Primatol 2016 Dec 8;78(12):1316-1325. Epub 2016 Jul 8.

Anthropologisches Institut, Universität Zürich, Zürich, Switzerland.

In group-living species with male dominance hierarchies where receptive periods of females do not overlap, high male reproductive skew would be predicted. However, the existence of female multiple mating and alternative male mating strategies can call into question single-male monopolization of paternity in groups. Ring-tailed lemurs (Lemur catta) are seasonally breeding primates that live in multi-male, multi-female groups. Although established groups show male dominance hierarchies, male dominance relationships can break down during mating periods. In addition, females are the dominant sex and mate with multiple males during estrus, including group residents, and extra-group males-posing the question of whether there is high or low male paternity skew in groups. In this study, we analyzed paternity in a population of wild L. catta from the Bezà Mahafaly Special Reserve in southwestern Madagascar. Paternity was determined with 80-95% confidence for 39 offspring born to nine different groups. We calculated male reproductive skew indices for six groups, and our results showed a range of values corresponding to both high and low reproductive skew. Between 21% and 33% of offspring (3 of 14 or three of nine, counting paternity assignments at the 80% or 95% confidence levels, respectively) were sired by extra-troop males. Males siring offspring within the same group during the same year appear to be unrelated. Our study provides evidence of varying male reproductive skew in different L. catta groups. A single male may monopolize paternity across one or more years, while in other groups, >1 male can sire offspring within the same group, even within a single year. Extra-group mating is a viable strategy that can result in extra-group paternity for L. catta males.
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http://dx.doi.org/10.1002/ajp.22584DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5129476PMC
December 2016

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

Primates 2016 Oct 6;57(4):541-7. Epub 2016 Jun 6.

Department of Anthropology, Center for the Advanced Study of Human Paleobiology, The George Washington University, Washington, DC, USA.

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.
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http://dx.doi.org/10.1007/s10329-016-0546-yDOI Listing
October 2016

Genetic Evidence for Male and Female Dispersal in Wild Lemur catta.

Folia Primatol (Basel) 2015 19;86(1-2):66-75. Epub 2015 May 19.

Lemur catta has traditionally been considered a species with male-biased dispersal; however, occasional female dispersal occurs. Using molecular data, we evaluated dispersal patterns in 2 L. catta populations in southwestern Madagascar: Tsimanampesotse National Park (TNP) and Bezà Mahafaly Special Reserve (BMSR). We also investigated the genetic differentiation between the populations and dispersal partner relatedness. Results showed minor genetic differentiation between the populations (ϴ(ST) = 0.039), which may indicate gene flow historically occurring in this region, made possible by the presence of L. catta groups between the sites. Different patterns of sex-biased dispersal were found between the sites using corrected assignment indices: male-biased dispersal in TNP, and a lack of sex-biased dispersal in BMSR. Observational evidence of female dispersal in BMSR supports these results and may imply intense female resource competition in and around BMSR, because small groups of 2-3 females have been observed dispersing within BMSR and entering the reserve from outside. These dispersing groups largely consisted of mothers transferring with daughters, although we have an aunt-niece pair transferring together. Genetic data suggest that males also transfer with relatives. Our data demonstrate that dispersal partners consist of same-sexed kin for L. catta males and females, highlighting the importance of kin selection.
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http://dx.doi.org/10.1159/000369386DOI Listing
March 2016

Model selection, zero-inflated models, and predictors of primate abundance in Korup National Park, Cameroon.

Am J Phys Anthropol 2012 Nov 18;149(3):417-25. Epub 2012 Sep 18.

Department of Sociology and Anthropology, James Madison University, MSC 7501, Harrisonburg, VA 22807, USA.

Determining the ecological and anthropogenic factors that shape the abundance and distribution of wild primates is a critical component of primate conservation research. Such research is complicated, however, whenever the species under study are encountered infrequently, a characteristic of many taxa that are threatened with extinction. Typically, the resulting data sets based on surveys of such species will have a high frequency of zero counts which makes it difficult to determine the predictor variables that are associated with species abundance. In this study, we test various statistical models using survey data that was gathered on seven species of primate in Korup National Park, Cameroon. Predictor variables include hunting signs and aspects of habitat structure and floristic composition. Our statistical models include zero-inflated models that are tailored to deal with a high frequency of zero counts. First, using exploratory data analysis we found the most informative set of models as ranked by Δ-AIC (Akaike's information criterion). On the basis of this analysis, we used five predictor variables to construct several regression models including Poisson, zero-inflated Poisson, negative binomial, and zero-inflated negative binomial. Total basal area of all trees, density of secondary tree species, hunting signs, and mean basal area of all trees were significant predictors of abundance in the zero-inflated models. We discuss the statistical logic behind zero-inflated models and provide an interpretation of parameter estimates. We recommend that researchers explore a variety of models when determining the factors that correlate with primate abundance.
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http://dx.doi.org/10.1002/ajpa.22139DOI Listing
November 2012

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

Am J Phys Anthropol 2012 Jan 3;147(1):21-9. Epub 2011 Nov 3.

Department of Social Sciences, University of Toronto at Scarborough, ON, Canada.

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.
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http://dx.doi.org/10.1002/ajpa.21603DOI Listing
January 2012

Linking genotypes, phenotypes, and fitness in wild primate populations.

Evol Anthropol 2011 May-Jun;20(3):104-19

Yale University, USA.

In the decade since the first draft of the human genome was announced, 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. 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.
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http://dx.doi.org/10.1002/evan.20306DOI Listing
February 2012

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

Authors:
Richard R Lawler

Am J Phys Anthropol 2011 14;146 Suppl 53:63-85. Epub 2011 Oct 14.

Department of Sociology and Anthropology, MSC 7501, Sheldon Hall, James Madison University, Harrisonburg, VA 22807, USA.

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.
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http://dx.doi.org/10.1002/ajpa.21611DOI Listing
February 2012

Feeding competition, cooperation, and the causes of primate sociality: a commentary on Sussman et al.

Authors:
Richard R Lawler

Am J Primatol 2011 Jan;73(1):84-90

Anthropology Department, James Madison University, 71 Alumnae Drive, Harrisonburg, VA 22801, USA.

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http://dx.doi.org/10.1002/ajp.20869DOI Listing
January 2011

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

Authors:
Richard R Lawler

J Hum Evol 2009 Sep 12;57(3):321-5. Epub 2009 Aug 12.

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http://dx.doi.org/10.1016/j.jhevol.2009.07.001DOI Listing
September 2009

Demography of Verreaux's sifaka in a stochastic rainfall environment.

Oecologia 2009 Sep 16;161(3):491-504. Epub 2009 Jun 16.

Department of Anthropology, Boston University, Boston, MA 02215, USA.

In this study, we use deterministic and stochastic models to analyze the demography of Verreaux's sifaka (Propithecus verreauxi verreauxi) in a fluctuating rainfall environment. The model is based on 16 years of data from Beza Mahafaly Special Reserve, southwest Madagascar. The parameters in the stage-classified life cycle were estimated using mark-recapture methods. Statistical models were evaluated using information-theoretic techniques and multi-model inference. The highest ranking model is time-invariant, but the averaged model includes rainfall-dependence of survival and breeding. We used a time-series model of rainfall to construct a stochastic demographic model. The time-invariant model and the stochastic model give a population growth rate of about 0.98. Bootstrap confidence intervals on the growth rates, both deterministic and stochastic, include 1. Growth rates are most elastic to changes in adult survival. Many demographic statistics show a nonlinear response to annual rainfall but are depressed when annual rainfall is low, or the variance in annual rainfall is high. Perturbation analyses from both the time-invariant and stochastic models indicate that recruitment and survival of older females are key determinants of population growth rate.
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http://dx.doi.org/10.1007/s00442-009-1382-1DOI Listing
September 2009

Testing for a historical population bottleneck in wild Verreaux's sifaka (Propithecus verreauxi verreauxi) using microsatellite data.

Authors:
Richard R Lawler

Am J Primatol 2008 Oct;70(10):990-4

Department of Anthropology, Boston University, Boston, Massachusetts 02215, USA.

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 Verreaux's 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.
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http://dx.doi.org/10.1002/ajp.20579DOI Listing
October 2008

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

Authors:
Richard R Lawler

Am J Phys Anthropol 2008 Jun;136(2):204-13

Department of Anthropology, Boston University, Boston, MA 02215, USA.

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 Verreaux's 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.
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http://dx.doi.org/10.1002/ajpa.20795DOI Listing
June 2008

A comparison of salivary pH in sympatric wild lemurs (Lemur catta and Propithecus verreauxi) at Beza Mahafaly Special Reserve, Madagascar.

Am J Primatol 2008 Apr;70(4):363-71

Department of Anthropology, University of North Dakota, Grand Forks, North Dakota 58202-8374, USA.

Chemical deterioration of teeth is common among modern humans, and has been suggested for some extinct primates. Dental erosion caused by acidic foods may also obscure microwear signals of mechanical food properties. Ring-tailed lemurs at the Beza Mahafaly Special Reserve (BMSR), Madagascar, display frequent severe tooth wear and subsequent tooth loss. In contrast, sympatric Verreaux's sifaka display far less tooth wear and infrequent tooth loss, despite both species regularly consuming acidic tamarind fruit. We investigated the potential impact of dietary acidity on tooth wear, collecting data on salivary pH from both species, as well as salivary pH from ring-tailed lemurs at Tsimanampesotse National Park, Madagascar. We also collected salivary pH data from ring-tailed lemurs at the Indianapolis Zoo, none of which had eaten for at least 12 hr before data collection. Mean salivary pH for the BMSR ring-tailed lemurs (8.098, n=41, SD=0.550) was significantly more alkaline than Verreaux's sifaka (7.481, n=26, SD=0.458). The mean salivary pH of BMSR (8.098) and Tsimanampesotse (8.080, n=25, SD=0.746) ring-tailed lemurs did not differ significantly. Salivary pH for the Indianapolis Zoo sample (8.125, n=16, SD=0.289) did not differ significantly from either the BMSR or Tsimanampesotse ring-tailed lemurs, but was significantly more alkaline than the BMSR Verreaux's sifaka sample. Regardless of the time between feeding and collection of pH data (from several minutes to nearly 1 hr), salivary pH for each wild lemur was above the "critical" pH of 5.5, below which enamel demineralization occurs. Thus, the high pH of lemur saliva suggests a strong buffering capacity, indicating the impact of acidic foods on dental wear is short-lived, likely having a limited effect. However, tannins in tamarind fruit may increase friction between teeth, thereby increasing attrition and wear in lemurs. These data also suggest that salivary pH varies between lemur species, corresponding to broad dietary categories.
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http://dx.doi.org/10.1002/ajp.20500DOI Listing
April 2008

Fitness and extra-group reproduction in male Verreaux's sifaka: An analysis of reproductive success from 1989-1999.

Authors:
Richard R Lawler

Am J Phys Anthropol 2007 Feb;132(2):267-77

Department of Anthropology, Boston University, Boston, MA 02215, USA.

Adult males in social groups often compete with other male group members for access to adult females. In some primate species, males also seek mating opportunities in neighboring social groups. Such extra-group fertilizations (EGFs) provide an additional source of variation in male fitness. This additional component of fitness provided by EGFs must be incorporated into analyses that investigate sources of variation in male lifetime reproductive success. In this study, a model is analyzed in which male fitness over a 10-year sample period is decomposed into additive and multiplicative variance and covariance components. The data come from an ongoing study of a wild population of Verreaux's sifaka (Propithecus verreauxi verreauxi) located at Beza Mahafaly Special Reserve, Southwest Madagascar. Paternity and demographic data for 134 males are used to decompose male fitness into the following three multiplicative components: reproductive lifespan during sample period, fertility, and offspring survival. These multiplicative components are estimated for males reproducing within their resident groups plus (i.e., the additive portion) for males reproducing in neighboring social groups. The analysis shows that variation in fertility makes the largest contribution to variation in total fitness, followed by variation in amount of time spent in sample period (which is a proxy of total reproductive lifespan) and variation in offspring survival. EGFs contribute an important source of variation to male fitness, and numerous factors enhance the opportunities for EGFs in male sifaka. These include female choice, a high degree of home range overlap, and a limited mating season.
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http://dx.doi.org/10.1002/ajpa.20507DOI Listing
February 2007

The locomotor behavior of Callicebus brunneus and Callicebus torquatus.

Folia Primatol (Basel) 2006 ;77(3):228-39

Department of Anthropology, Boston University, MA 02215, USA.

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.
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http://dx.doi.org/10.1159/000091232DOI Listing
June 2006

Sifaka positional behavior: ontogenetic and quantitative genetic approaches.

Authors:
Richard R Lawler

Am J Phys Anthropol 2006 Oct;131(2):261-71

Department of Anthropology, Boston University, Massachusetts 02215, USA.

In many primate species, hands and feet are large relative to neonatal body weight, and they subsequently exhibit negative allometric growth during ontogeny. Here, data are presented showing that this pattern holds for a wild population of lemur, Verreaux's sifaka (Propithecus verreauxi verreauxi). Using morphometric data collected on this population, it is shown that younger animals possess relatively large hands and feet. This ontogenetic pattern suggests a simple behavioral test: do juvenile animals with their larger, almost adult-sized hands and feet locomote on similarly sized substrates as adult animals? Using locomotor bout sampling, this question was tested by collecting positional behavior data on this population. Results from this test find no differences in locomotor behaviors or substrate use between yearlings and adult animals. To place these results in a broader evolutionary context, heritabilities and selection gradients of hands, feet, and other limb elements for animals in this population were estimated. Among limb elements, heritabilities range from 0.16-0.44, with the foot having the lowest value. Positive directional selection acts most strongly on the foot (directional selection gradient = 0.119). The low heritability and positive selection coefficient indicate that selection has acted, and continues to act, on foot size in young animals. These results are interpreted within a functional context with respect to the development of locomotor coordination: larger feet enable young animals to use "adult-sized" substrates when they move through their habitat. It is suggested that the widespread pattern of negative allometry of the extremities in sifaka and other primates is maintained by selection, and does not simply reflect a primitive developmental pathway that has no adaptive basis.
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http://dx.doi.org/10.1002/ajpa.20430DOI Listing
October 2006

Intrasexual selection in Verreaux's sifaka (Propithecus verreauxi verreauxi).

J Hum Evol 2005 Mar 20;48(3):259-77. Epub 2005 Jan 20.

Department of Anthropology, Boston University, Boston, MA 02215, USA.

Studies of sexual selection show that both female choice and male-male competition can influence the evolution and expression of male phenotypes. In this regard, it is important to determine the functional basis through which male traits influence variation in male reproductive success. In this study, we estimate the strength and type of sexual selection acting on adult males in a population of wild lemur, Verreaux's sifaka (Propithecus verreauxi verreauxi). The data used in this study were collected at Beza Mahafaly Special Reserve, southwest Madagascar. We conducted paternity analyses on 70 males in order to estimate the distribution of reproductive success in this population. Paternity data were combined with morphometric data in order to determine which morphological traits covary with male fitness. Five morphological traits were defined in this analysis: body size, canine size, torso shape, arm shape, and leg shape. We utilized phenotypic selection models in order to determine the strength and type of selection acting directly on each trait. Our results show that directional selection acts on leg shape (a trait that is functionally related to locomotor performance), stabilizing selection acts on body mass and torso shape, and negative correlational selection acts on body mass and leg shape. We draw from biomechanical and kinematic studies of sifaka locomotion to provide a functional context for how these traits influence male mating competition within an arboreal environment. Verreaux's sifaka and many other gregarious lemurs are sexually monomorphic in body mass and canine size, despite a high frequency and intensity of male-male aggressive competition. Our results provide some insight into this paradox: in our population, there is no directional selection acting on body mass or canine size in males. The total pattern of selection implicates that behaviors relating to locomotor performance are more important than behaviors relating to fighting ability during intrasexual contests.
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http://dx.doi.org/10.1016/j.jhevol.2004.11.005DOI Listing
March 2005

Genetic population structure of the white sifaka (Propithecus verreauxi verreauxi) at Beza Mahafaly Special Reserve, southwest Madagascar (1992-2001).

Mol Ecol 2003 Sep;12(9):2307-17

Department of Anthropology, Yale University, New Haven CT 06511, USA.

Gene flow within and between social groups is contingent on behaviourally mediated patterns of mating and dispersal. To understand how these patterns affect the genetic structure of primate populations, long-term data are required. In this study, we analyse 10 years of demographic and genetic data from a wild lemur population (Propithecus verreauxi verreauxi) at Beza Mahafaly Special Reserve, southwest Madagascar. Our goal is to specify how patterns of mating and dispersal determine kinship and genetic diversity among animals in the population. Specifically, we use microsatellite, parentage, and census data to obtain estimates of genetic subdivision (FST), within group homozygosity (FIS), and relatedness (r) within and among social groups in the population. We analyse different classes of individuals (i.e. adults, offspring, males, females) separately in order to discern which classes most strongly influence aspects of population structure. Microsatellite data reveal that, across years, offspring are consistently more heterozygous than expected within social groups (FIS mean = -0.068) while adults show both positive and negative deviations from expected genotypic frequencies within groups (FIS mean = 0.003). Offspring cohorts are more genetically subdivided than adults (FST mean = 0.108 vs. 0.052) and adult females are more genetically subdivided than adult males (FST mean = 0.098 vs. 0.046). As the proportion of females in social groups increases, the proportion of offspring sired by resident males decreases. Offspring are characterized by a heterozygote excess as resident males (vs. nonresident males) sire the majority of offspring within groups. We link these genetic data to patterns of female philopatry, male dispersal, exogamy, and offspring sex-ratio. Overall, these data reveal how mating and dispersal tactics influence the genetic population structure in this species.
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http://dx.doi.org/10.1046/j.1365-294x.2003.01909.xDOI Listing
September 2003

The relationship between tail use and positional behavior in Alouatta palliata.

Primates 2002 Apr;43(2):147-52

Department of Anthropology, P. O. Box 208277, New Haven, Connecticut 06520-8277, USA.

The relationship between tail use and positional behavior is explored in Alouatta palliata. During bridging, climbing, suspension, standing, and sprawling, the tail is attached to a substrate for the majority of sample points. Tail attachment was more likely to occur when the animal is traveling on vertical or terminal substrates. Quadrupedalism showed few instances of attachment and sitting reflected nearly equal amounts of prehension and non-prehension. Tail prehension is used in all behavioral contexts but shows higher frequencies of attachment during feeding than during resting, or foraging. Tail prehension appears to aid in the stability, support, and balance of the animal across numerous positional behaviors.
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http://dx.doi.org/10.1007/BF02629675DOI Listing
April 2002
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