Andrew S. Burrell

Successive radiations, not stasis, in the South American primate fauna

The earliest Neotropical primate fossils complete enough for taxonomic assessment, Dolichocebus, Tremacebus, and Chilecebus, date to approximately 20 Ma. These have been interpreted as either closely related to extant forms or as extinct stem lineages. The former hypothesis of morphological stasis requires most living platyrrhine genera to have diverged before 20 Ma. To test this hypothesis, we collected new complete mitochondrial genomes from Aotus lemurinus, Saimiri sciureus, Saguinus oedipus, Ateles belzebuth, and Callicebus donacophilus. We combined these with published sequences from Cebus albifrons and other primates to infer the mitochondrial phylogeny. We found support for a cebid/atelid clade to the exclusion of the pitheciids. Then, using Bayesian methods and well-supported fossil calibration constraints, we estimated that the platyrrhine most recent common ancestor (MRCA) dates to 19.5 Ma, with all major lineages diverging by 14.3 Ma. Next, we estimated catarrhine divergence dates on the basis of platyrrhine divergence scenarios and found that only a platyrrhine MRCA less than 21 Ma is concordant with the catarrhine fossil record. Finally, we calculated that 33% more change in the rate of evolution is required for platyrrhine divergences consistent with the morphologic stasis hypothesis than for a more recent radiation. We conclude that Dolichocebus, Tremacebus, and Chilecebus are likely too old to be crown platyrrhines, suggesting they were part of an extinct early radiation. We note that the crown platyrrhine radiation was concomitant with the radiation of 2 South American xenarthran lineages and follows a global temperature peak and tectonic activity in the Andes.

Primate phylogenetic relationships and divergence dates inferred from complete mitochondrial genomes.

The origins and the divergence times of the most basal lineages within primates have been difficult to resolve mainly due to the incomplete sampling of early fossil taxa. The main source of contention is related to the discordance between molecular and fossil estimates: while there are no crown primate fossils older than 56Ma, most molecule-based estimates extend the origins of crown primates into the Cretaceous. Here we present a comprehensive mitogenomic study of primates. We assembled 87 mammalian mitochondrial genomes, including 62 primate species representing all the families of the order. We newly sequenced eleven mitochondrial genomes, including eight Old World monkeys and three strepsirrhines. Phylogenetic analyses support a strong topology, confirming the monophyly for all the major primate clades. In contrast to previous mitogenomic studies, the positions of tarsiers and colugos relative to strepsirrhines and anthropoids are well resolved. In order to improve our understanding of how fossil calibrations affect age estimates within primates, we explore the effect of seventeen fossil calibrations across primates and other mammalian groups and we select a subset of calibrations to date our mitogenomic tree. The divergence date estimates of the Strepsirrhine/Haplorhine split support an origin of crown primates in the Late Cretaceous, at around 74Ma. This result supports a short-fuse model of primate origins, whereby relatively little time passed between the origin of the order and the diversification of its major clades. It also suggests that the early primate fossil record is likely poorly sampled.

Conservation Implications of Hybridization in African Cercopithecine Monkeys

Numerous field reports of hybrid monkeys and documented cases of persistent hybrid zones suggest that natural hybridization is common among African cercopithecines. Both theoretical considerations and a review of cases lead us to conclude that parapatric hybridization among closely related allotaxa is a widespread, usually natural process whose incidence may be modified by human influence. Sympatric hybridization, between species ecologically distinct enough to have overlapping ranges, is rarer, and in monkeys tends to occur in settings where natural or anthropogenic habitat edges restrict migration and hence access to unrelated conspecific mates. Although sympatric hybridization occurs in the absence of human disturbance, and may even have been a creative force in cercopithecine evolution, anthropogenic habitat fragmentation may increase its incidence. Hybridization with a more abundant form may increase the level of threat faced by a species whose numbers and range have been severely restricted, either naturally or artificially.

Mitochondrial evidence for the hybrid origin of the kipunji, Rungwecebus kipunji (Primates: Papionini)

Common baboons (Papio), gelada baboons (Theropithecus) and baboon-mangabeys (Lophocebus) are closely related African papionin monkeys. In 2005, the species Lophocebus kipunji was described from relict montane and submontane forests in Tanzania, based upon a single specimen and observations of living animals. Its initial assignment to Lophocebus was based on its overall morphology, but subsequent genetic studies suggesting that it was sister taxon to common baboons (Papio) led to its generic separation, as Rungwecebus. As a mangabey-like sister-taxon to Papio, Rungwecebus could be interpreted either as an arboreal derivative from a more terrestrial, baboon-like ancestor, or as a survivor of a mangabey-like common ancestor of the Lophocebus-Papio-Theropithecus clade. Here, we present a new, strongly-supported, mitochondrial DNA (mtDNA) phylogeny that includes Papio baboons from populations geographically close to the kipunji. Rather than supporting sister-taxon status, the new phylogeny not only situates the kipunjis mtDNA among Papio haplotypes, it clearly assigns it to a mitochondrial clade including geographically adjacent yellow baboons (Papio cynocephalus). This relationship suggests either that the kipunji is descended from a yellow baboon, and has converged on a mangabey-like morphology, or, much more likely, that it originated by hybridization between Papio cf.cynocephalus females and Lophocebus sp. males, about 0.65 Ma. We believe this to be the first case among mammals in which a natural occurrence of inter-generic hybridization can be shown to have resulted in a new, distinct, long-surviving taxon. More such cases can be anticipated as molecular evidence accumulates.

Kinda baboons (Papio kindae) and grayfoot chacma baboons (P. ursinus griseipes) hybridize in the Kafue river valley, Zambia

The ranges of small kinda (Papio kindae) and much larger grayfooted chacma (P. ursinus griseipes) baboons adjoin in the Kafue National Park, Zambia. In a visual survey of baboons at 48 sites in the Kafue River drainage we found that, contrary to previous reports, groups at the species interface near the town of Ngoma are phenotypically diverse and presumably formed by multigenerational hybridization. Mitochondrial and/or Y‐chromosome genetic markers from fecal samples (N=164) collected at 29 sites support this conclusion. Groups with phenotypic signs of a history of hybridization also had taxon‐specific mitochondria and Y‐haplotypes from both parental species. Although the distribution of mitochondrial haplotypes largely mirrored that of external phenotypes, a significant proportion of male specimens from grayfoot as well as hybrid groups carried kinda Y‐chromosomes, and kinda Y‐chromosomes were involved in all observed cases of mitochondrial/Y‐chromosome discordance. These observations are consistent with, though they do not prove, a population history in which the range of chacmas and the hybrid zone have advanced at the expense of the kinda range. They also suggest that, unexpectedly, kinda male×chacma female matings are much more common than the reciprocal cross in the ancestry of hybrids. We suggest that distinctive male kinda behavior and the “juvenile” appearance of kinda baboons of both sexes, perhaps combined with obstetric difficulties of a small kinda female carrying the large offspring of a chacma male, may account for this bias. Am. J. Primatol. 73:291–303, 2011.

Lesula: A New Species of Cercopithecus Monkey Endemic to the Democratic Republic of Congo and Implications for Conservation of Congo’s Central Basin

In June 2007, a previously undescribed monkey known locally as “lesula” was found in the forests of the middle Lomami Basin in central Democratic Republic of Congo (DRC). We describe this new species as Cercopithecus lomamiensis sp. nov., and provide data on its distribution, morphology, genetics, ecology and behavior. C. lomamiensis is restricted to the lowland rain forests of central DRC between the middle Lomami and the upper Tshuapa Rivers. Morphological and molecular data confirm that C. lomamiensis is distinct from its nearest congener, C. hamlyni, from which it is separated geographically by both the Congo (Lualaba) and the Lomami Rivers. C. lomamiensis, like C. hamlyni, is semi-terrestrial with a diet containing terrestrial herbaceous vegetation. The discovery of C. lomamiensis highlights the biogeographic significance and importance for conservation of central Congo’s interfluvial TL2 region, defined from the upper Tshuapa River through the Lomami Basin to the Congo (Lualaba) River. The TL2 region has been found to contain a high diversity of anthropoid primates including three forms, in addition to C. lomamiensis, that are endemic to the area. We recommend the common name, lesula, for this new species, as it is the vernacular name used over most of its known range.

The stem catarrhine Saadanius does not inform the timing of the origin of crown catarrhines

A precise knowledge of the divergence time between Hominoidea (apes and humans) and Cercopithecoidea (Old World monkeys) has been hampered by the paucity of fossils between the early Miocene (23Ma) and the early Oligocene (30Ma). The earliest known Old World monkey is represented by Victoriapithecus macinnesi from Kenya, dated to 19 Ma (Benefit and McCrossin, 2002; Pilbeam and Walker, 1968), while several potential early hominoid fossils are dated to around 20 Ma, including Proconsul at 20e22.5 Ma (Harrison, 2010; Harrison and Andrews, 2009), Morotopithecus at 20 Ma (Gebo et al., 1997), and Ugandapithecus at 19e20 Ma (Senut et al., 2000). Kamoyapithecus, only known from some isolated dentition, dates back to the late Oligocene (23.9e27.8 Ma); however, its phylogenetic position remains controversial and not all authors classify it as a crown catarrhine (Harrison, 2002; Leakey et al., 1995). Based on this evidence in the fossil record, the divergence between hominoids and cercopithecoids is understood to be older than 20 Mya and most molecular estimates of primate divergences have used this as a calibration point (Chatterjee et al., 2009; Fabre et al., 2009; Hodgson et al., 2009; Raaum et al., 2005; Steiper and Young, 2008) In a recent study, Zalmout et al. (2010) describe a new Oligocene primate from Saudi Arabia, which they claim provides new insights into the time of divergence between apes and Old World monkeys. The newly described fossil, named Saadanius hijazensis and dated to w29Ma, is inferred to be a stem catarrhine, closely related to living apes and Old World monkeys (crown Catarrhini). According to the authors, this finding indicates an origin for crown Catarrhini after

A New Method for Genome-wide Marker Development and Genotyping Holds Great Promise for Molecular Primatology

Over the last two decades primatologists have benefited from the use of numerous molecular markers to study various aspects of primate behavior and evolutionary history. However, most of the studies to date have been based on a single locus, usually mitochondrial DNA, or a few nuclear markers, e.g., microsatellites. Unfortunately, the use of such markers not only is unable to address successfully important questions in primate population genetics and phylogenetics (mainly because of the discordance between gene tree and species tree), but also their development is often a time-consuming and expensive task. The advent of next-generation sequencing allows researchers to generate large amounts of genomic data for nonmodel organisms. However, whole genome sequencing is still cost prohibitive for most primate species. We here introduce a second-generation sequencing technique for genotyping thousands of genome-wide markers for nonmodel organisms. Restriction site–associated DNA sequencing (RAD-seq) reduces the complexity of the genome and allows inexpensive and fast discovery of thousands of markers in many individuals. Here, we describe the principles of this technique and we demonstrate its application in five primates, Microcebus sp., Cebus sp., Theropithecus gelada, Pan troglodytes, and Homo sapiens, representing some of the major lineages within the order. Despite technical and bioinformatic challenges, RAD-seq is a promising method for multilocus phylogenetic and population genetic studies in primates, particularly in young clades in which a high number of orthologous regions are likely to be found across populations or species.

Genetic signatures of a demographic collapse in a large-bodied forest dwelling primate (Mandrillus leucophaeus).

It is difficult to predict how current climate change will affect wildlife species adapted to a tropical rainforest environment. Understanding how population dynamics fluctuated in such species throughout periods of past climatic change can provide insight into this issue. The drill (Mandrillus leucophaeus) is a large-bodied rainforest adapted mammal found in West Central Africa. In the middle of this endangered monkeys geographic range is Lake Barombi Mbo, which has a well-documented palynological record of environmental change that dates to the Late Pleistocene. We used a Bayesian coalescent-based framework to analyze 2,076 base pairs of mitochondrial DNA across wild drill populations to infer past changes in female effective population size since the Late Pleistocene. Our results suggest that the drill underwent a nearly 15-fold demographic collapse in female effective population size that was most prominent during the Mid Holocene (approximately 3-5 Ka). This time period coincides with a period of increased dryness and seasonality across Africa and a dramatic reduction in forest coverage at Lake Barombi Mbo. We believe that these changes in climate and forest coverage were the driving forces behind the drill population decline. Furthermore, the warm temperatures and increased aridity of the Mid Holocene are potentially analogous to current and future conditions faced by many tropical rainforest communities. In order to prevent future declines in population size in rainforest-adapted species such as the drill, large tracts of forest should be protected to both preserve habitat and prevent forest loss through aridification.

Panmixia postponed: ancestry-related assortative mating in contemporary human populations.

A study of two different populations reveals that in both the choice of a spouse is non-random not only in respect of broad ethnic group but also in regard to specific ancestries within that group. The cause of this surprising bias remains unclear.