Ontogeny and phylogeny of mating behaviour: social heteroch rony in primates.

Based on the Recognition Concept of species, the specific-mate contact model posits that mating systems develop as combinations of two fundamental courtship strategies that we interpret here in terms of behavioural heterochrony: territorial mate-attraction evolved as an effect of peramorphosis whereas group-living mate-seeking evolved as an effect of paedomorphosis. We tested this hypothesis on primates in a phylogenetic and paleo-climatic context. Our results suggest that primate promiscuity (both males and females are mate-seekers) evolved with group-living from ancestral pair-living monogamy (both males and females are mate-attractors) in the Palaeogene, as the result of a slowdown in growth (neoteny) caused by increased environmental predictability. A secondary return to territorial monogamy probably evolved as the result of accelerated growth driven by seasonality (acceleration). Polygamy evolved in the Neogene during periods of forest fragmentation and environmental unpredictability. Small monogamous ancestors evolved seasonal polyandry (female attraction) as an effect of truncated development (progenesis). Large promiscuous, neotenic ancestors evolved non-seasonal polygyny (male attraction) as an effect of prolonged development (hypermorphosis) in males. We conclude that social heterochrony offers alternative explanations for the coevolution of life history and mating be-haviour; and we discuss the implications of our model for human social evolution.

The evolution of palate shape in the Lepilemur-Cheirogaleidae clade (Primates: Strepsirrhini).

OBJECTIVES: Phylogenies consistently group the folivorous Lepilemur species with the small-bodied insectivorous-frugivorous cheirogaleids. Juvenile lepilemurs and adult cheirogaleids share allometries in most aspects of skull morphology, except the palate. We investigated potential influences on palate shape in these taxa and several outgroups using geometric morphometrics. MATERIALS AND METHODS: Our sample included representatives of four extant strepsirrhine families, Cheirogaleidae (including Lepilemurinae), Lemuridae, Indriidae, and Galagidae, and one subfossil Megaladapis. Our dataset comprised 32 landmarks collected from 397 specimens representing 15 genera and 28 species, and was analyzed using generalized procrustes analyses and between group principal component analysis. We explored the influence of size, phylogeny, diet, and the propagation of loud vocalizations on palate shape. RESULTS: While congeneric species clustered within the morphospace, the phylomorphospace did not mirror molecular phylogenetic hypotheses of higher-order relationships. Four palate forms were distinguished within the Cheirogaleidae. Diet, strongly linked to body size, had the single greatest influence on palate shape. The production of long-distance advertisement calls was most often associated with positive scores on the PC1 axis. DISCUSSION: Our results suggest that the extensive variation in palate shape among Cheirogaleidae is related to dietary shifts that accompanied changes in body size during the clade's radiation. Molecular phylogenies indicate that cheirogaleid diversification involved repeated dwarfing events, which in turn drove dietary shifts from ancestral folivory-frugivory to frugivory, gummivory, and faunivory in the descendant species. The elongated Lepilemur palate is probably related to accelerated eruption of the cheek teeth to render juveniles competent to shear leaves upon weaning.

Sharing the burden: A neutral approach to socioecological theory.

OBJECTIVE: The socioecological model (SEM) is a popular collection of controversial models purporting to explain mating systems in terms of ecological and social parameters. Despite its guise of objectivity, several of its hypotheses assume Victorian gender stereotypes of active, competing males heedlessly sowing their seeds, and cautious, passive females, imprisoned by greater costs of reproduction and their consequent resourceߚdependence. METHODS: We enter this debate by taking a previously neglected explanatory approach borrowed from species theory. According to the Recognition Concept of sexual species, the unit of reproductive success/fitness is irreducible to fewer than two integrated subparts (minimally a male and a female). Phyletic changes in mating systems logically effect changes in fertilization systems, leading to reproductive isolation. We take our primary assumption of the average equivalence of female and male contributions to successful reproduction from the writings of the natural philosopher, Antoinette Blackwell. RESULTS: We revisit the SEM with its contradictions and extrapolations, and develop a genderߚneutral alternative hypothesis termed SpecificߚMate Contact (SMC), centered on two fundamental mating strategies: sexual animals may behave as synchronous mateߚattractors or asynchronous mateߚseekers, generating four possible mating system combinations (monogamy: two attractors; promiscuity: two seekers; polygyny: male attractor and female seeker; polyandry: female attractor and male seeker). CONCLUSIONS: Our approach predicts all known primate mating systems using a neutral (nonߚsexist) principle. The approach is also neutral in the sense that it does not invoke either competition or cooperation: fertilization success is considered a posteriori and males and females are coߚadapted to this end rather than cognitively cooperative.

The evolution of the Cercopithecini: a (post)modern synthesis.

The Cercopithecini, or African guenon monkeys, are one of the most diverse clades of living primates and comprise the most species-rich clade of Catarrhini. Species identity is announced by flamboyant coloration of the facial and genital regions and, more cryptically, by vigorous chromosomal rearrangements among taxa. Beneath the skin, however, these animals are skeletally conservative and show low levels of genetic sequence divergence consonant with recent divergence between congeneric species. The guenons clearly demonstrate that morphological, cytogenetic, and reproductive differentiation proceed at different rates during speciation. We review diverse kinds of data in an effort to understand this conundrum.

A giant among dwarfs: a new species of galago (Primates: Galagidae) from Angola.

OBJECTIVES: Based on vocalization recordings of an unknown galago species, our main objectives were to compare morphology and call structure with known closely-related taxa and describe a new species of galago. MATERIALS AND METHODS: We conducted field surveys in three forest habitats along the escarpment region in western Angola (Kumbira Forest, Bimbe Area, and Northern Scarp Forest), and examined galago specimens from museums worldwide. We digitized and analyzed calls using Avisoft SASLab Pro software. We also compared museum specimens from Angola with other Galago and Galagoides specimens, and conducted comparative analyses (ANOVA and between group principle component analysis) based on a set of twelve linear measurements of skulls and teeth. RESULTS: We describe the new species to which we give the name Angolan dwarf galago, Galagoides kumbirensis sp. nov. The new species has a loud and characteristic crescendo call, used by other Galagoides spp. (sensu stricto) in West Africa to attract companions and repel rivals. However, this call shows species-typical differences from its closest relatives. Galagoides kumbirensis sp. nov. is also distinguished by differences in the skull morphology, pelage color and facial markings, as well as a larger body size, similar to that of Galago moholi, which is not known to be sympatric. CONCLUSION: This discovery points to the importance of Angolan forests as refuges for endemic biodiversity. These forests are under severe threat from overexploitation, and there is an urgent need to establish conservation measures and designate protected areas.

Characterizing cryptic species: A morphometric analysis of craniodental characters in the dwarf galago genus Galagoides.

OBJECTIVES: The true dwarf galagos of the genus Galagoides, G. demidoff and G. thomasi, are difficult to distinguish morphologically at a specific or subspecific level, and most taxonomic designations are based primarily on geographic localities. We used morphometrics to investigate the morphological diversity of the genus. MATERIALS AND METHODS: We conducted statistical analyses of 12 linear measurements on 290 Galagoides skulls housed in museums worldwide, and assembled body weights for 71 wild caught specimens. We examined sexual dimorphism and specific and subspecific distinctiveness using MANOVA, ANOVA, principle components analysis and canonical variate analysis. RESULTS: We distinguished skulls identified as Galagoides demidoff and G. thomasi with ∼70% reliability, and demonstrated consistently different patterns of static allometry in craniodental variables. Variables supporting specific distinction included M1 width, palate width at P2 , palate (snout) length, length of premaxillary tube, width across mastoids, and total skull length. The type specimens of G. orinus and G. rondoensis were significantly different from G. demidoff and G. thomasi, but grouped with them in a CVA including G. zanzibaricus and G. granti, although molecular studies indicate that their true affiliation is with the latter species. Subspecies within G. demidoff could not be distinguished using craniodental morphometrics. DISCUSSION: Galagoides demidoff and G. thomasi can be distinguished relatively reliably, and are broadly sympatric across western and central Africa. Neither species showed evidence of sexual dimorphism in craniodental size or shape. Size variation has a greater influence on skull morphology in G. demidoff than it has on G. thomasi. Am J Phys Anthropol 158:288-299, 2015. © 2015 Wiley Periodicals, Inc.

A multilocus phylogeny reveals deep lineages within African galagids (Primates: Galagidae).

BACKGROUND: Bushbabies (Galagidae) are among the most morphologically cryptic of all primates and their diversity and relationships are some of the most longstanding problems in primatology. Our knowledge of galagid evolutionary history has been limited by a lack of appropriate molecular data and a paucity of fossils. Most phylogenetic studies have produced conflicting results for many clades, and even the relationships among genera remain uncertain. To clarify galagid evolutionary history, we assembled the largest molecular dataset for galagos to date by sequencing 27 independent loci. We inferred phylogenetic relationships using concatenated maximum-likelihood and Bayesian analyses, and also coalescent-based species tree methods to account for gene tree heterogeneity due to incomplete lineage sorting. RESULTS: The genus Euoticus was identified as sister taxon to the rest of the galagids and the genus Galagoides was not recovered as monophyletic, suggesting that a new generic name for the Zanzibar complex is required. Despite the amount of genetic data collected in this study, the monophyly of the family Lorisidae remained poorly supported, probably due to the short internode between the Lorisidae/Galagidae split and the origin of the African and Asian lorisid clades. One major result was the relatively old origin for the most recent common ancestor of all living galagids soon after the Eocene-Oligocene boundary. CONCLUSIONS: Using a multilocus approach, our results suggest an early origin for the crown Galagidae, soon after the Eocene-Oligocene boundary, making Euoticus one of the oldest lineages within extant Primates. This result also implies that one - or possibly more - stem radiations diverged in the Late Eocene and persisted for several million years alongside members of the crown group.

Life history traits, maternal behavior and infant development of blue-eyed black lemurs (Eulemur flavifrons).

An understanding of recruitment is important for estimating population growth and viability, and their implications for conservation. We present the first results regarding the life history, maternal behavior and infant development of the critically endangered blue-eyed black lemur (Eulemur flavifrons) of Madagascar. The species breeds seasonally, with births occurring at the end of the dry season, between late August and October. Over two successive birth seasons in 2006 and 2007, we observed a total of 13 lactating females and 22 infants from six groups. We inferred age at first reproduction as 3 years, and calculated the birth rate as 1.0 infant per female per year with a mean inter-birth interval of 358 ± 24.81 days (319-410 days). Infants spent the first 3 weeks of life constantly with their mothers; locomotor independence and ingestion of solid food began at week 10, and the infants were weaned by week 25. After week 28, infants spent less than 20% of their time in contact with their mothers. Over the study period infant mortality was 22.7%, with predation and sickness observed as causes. Our results suggest that overall recruitment is relatively slow, which has implications for the species' survival, particularly given their restricted and threatened habitat.

A population estimate of blue-eyed black lemurs in Ankarafa Forest, Sahamalaza-Iles Radama National Park, Madagascar.

The critically endangered blue-eyed black lemur (Eulemur flavifrons) has one of the smallest distributions of any lemur, occurring only in the north-western forests of Madagascar. We report the results of a population estimate of this taxon in part of the Ankarafa Forest, Sahamalaza-Iles Radama National Park, a dry deciduous forest. We collected data between September 2007 and February 2008 using a total count method with marked individuals and known groups. In all, 228 individuals comprising 29 groups were counted. Group sizes ranged from 4 to 11 individuals with a mean of 8 ± 1.8. We estimated population density to be 1.0 individual/ha or 97.3 individuals/km(2) for our study area, which is higher than previous estimates reported for Ankarafa and other sites within the Sahamalaza Peninsula. Our mean group size, however, was similar to those determined in previous studies. Both group size and density of the blue-eyed black lemur were higher within the National Park than in previous studies outside the Park.

Phylogenetic relationships among the Lorisoidea as indicated by craniodental morphology and mitochondrial sequence data.

The phylogeny of the Afro-Asian Lorisoidea is controversial. While postcranial data attest strongly to the monophyly of the Lorisidae, most molecular analyses portray them as paraphyletic and group the Galagidae alternately with the Asian or African lorisids. One of the problems that has bedevilled phylogenetic analysis of the group in the past is the limited number of taxa sampled for both ingroup families. We present the results of a series of phylogenetic analyses based on 635 base pairs (bp) from two mitochondrial genes (12S and 16S rRNA) with and without 36 craniodental characters, for 11 galagid and five lorisid taxa. The outgroup was the gray mouse lemur (Microcebus murinus). Analyses of the molecular data included maximum parsimony (MP), neighbor joining (NJ), maximum likelihood (ML), and Bayesian methods. The model-based analyses and the combined "molecules+morphology" analyses supported monophyly of the Lorisidae and Galagidae. The lorisids form two geographically defined clades. We find no support for the taxonomy of Galagidae as proposed recently by Groves [Primate Taxonomy, Washington, DC: Smithsonian Institution Press. 350 p, 2001]. The taxonomy of Nash et al. [International Journal of Primatology 10:57-80, 1989] is supported by the combined "molecules+morphology" analysis; however, the model-based analyses suggest that Galagoides may be an assemblage of species united by plesiomorphic craniodental characters.

A composite molecular phylogeny of living lemuroid primates.

Lemuroid phylogeny is a source of lively debate among primatologists. Reconstructions based on morphological, physiological, behavioural and molecular data have yielded a diverse array of tree topologies with few nodes in common. In the last decade, molecular phylogenetic studies have grown in popularity, and a wide range of sequences has been brought to bear on the problem, but consensus has remained elusive. We present an analysis based on a composite molecular data set of approx. 6,400 bp assembled from the National Center for Biotechnology Information (NCBI) database, including both mitochondrial and nuclear genes, and diverse analytical methods. Our analysis consolidates some of the nodes that were insecure in previous reconstructions, but is still equivocal on the placement of some taxa. We conducted a similar analysis of a composite data set of approx. 3,600 bp to investigate the controversial relationships within the family Lemuridae. Here our analysis was more successful; only the position of Eulemur coronatus remained uncertain.

Lack of torpor in free-ranging southern lesser galagos, Galago moholi: ecological and physiological considerations.

Studies investigating heterothermy under natural conditions are particularly scarce for tropical species. However, heterothermy patterns in tropical and subtropical environments often differ markedly from those observed in arctic and temperate species. The investigation of heterothermy in strepsirhine primates has focussed largely on the Malagasy cheirogaleids. In addition, a physiological verification of torpor occurrence in mainland strepsirhines is important with regard to arguments pertaining to the colonization of Madagascar by strepsirhine primates. We measured body temperatures of 11 free-ranging Galago moholi, between February 2002 and September 2003, for 3 consecutive months for each animal. No incidents of heterothermy were recorded throughout the study period. We considered how physiological and ecological aspects of G. moholi biology might have obviated the use of torpor. It was suggested that the breeding pattern observed in G. moholi prevented torpor use whilst increasing fecundity, and that the ecological costs of torpor far outweighed the energetic costs. This study highlights the need for more studies on free-ranging animals to elucidate the physiological, ecological and phylogenetic constraints and determinants of torpor use. Furthermore, if convincing arguments are to be made regarding the possible role of heterothermy in species dispersal, more data from free-ranging animals are needed.

Lack of congruence between morphological and molecular data in reconstructing the phylogeny of the galagonidae.

Published cladistic reconstructions of galagonid phylogeny based on morphological, behavioral, and genetic data have had few elements in common. A recent molecular study indicated that 2 of the 3 generic groupings derived from morphological data were not consistent with tree topologies constructed from the analysis of mitochondrial DNA sequences. In this study, we compiled and analyzed a data set based on craniodental morphology in 13 galagonid and 8 outgroup taxa, comprising 3 dwarf-lemur and 5 loris species, and subjected it to cladistic analysis. Our aim was not only to generate a new phylogenetic hypothesis based on these data, but also to investigate the conditions under which congruence could be achieved between these results and those obtained previously. The data set was found to be highly sensitive to the choice of outgroup, with the lorises showing high interspecific variability in cranial structure. Congruence between the craniodental and molecular trees could be achieved only if Arctocebus was used as the outgroup and two characters were preferentially weighted. Further progress in the reconstruction of galagonid phylogeny will require seeking consensus in a variety of other data sets, including postcranial morphology, behavior, and additional gene sequences. The effect of different outgroups on molecular analysis needs attention.

Distribution of erythrocytic allozymes in two sibling species of greater galago [Galago crassicaudatus E. Geoffroy 1812 and G. garnettii (Ogilby 1838)].

This study investigated the use of erythrocyte enzymes as indicators of the presence or absence of gene flow between the sibling species G. crassicaudatus and G. garnettii. Fifty-five animals deriving from 14 different source populations were included in the analyses. In addition to hemoglobin, eight enzyme systems were examined: acid phosphatase, adenylate kinase, carbonic anhydrase II, esterase D, glucose-6-phosphate dehydrogenase, 6-phosphogluconate dehydrogenase, peptidase A, and peptidase B. of these, adenylate kinase, glucose-6-phosphate dehydrogenase, hemoglobin, peptidase A, and peptidase B showed no interspecific or intraspecific variation. Esterase D was polymorphic in certain populations of G. crassicaudatus but not in others or in G. garnettii. Acid phosphatase and 6-phosphogluconate dehydrogenase were polymorphic in G. garnettii but monomorphic in all G. crassicaudatus populations. The taxa showed fixation for different alleles at the carbonic anhydrase II locus, indicating a lack of gene exchange between the taxa. We suggest that acid phosphatase, 6-phosphogluconate dehydrogenase, and carbonic anhydrase II may be used as genetic markers in the identification of these two taxa.