Primate phylogeny, evolutionary rate variations, and divergence times: a contribution from the nuclear gene IRBP

The first third (ca. 1200 bp) of exon 1 of the nuclear gene encoding the interstitial retinoid-binding protein (IRBP) has been sequenced for 12 representative primates belonging to Lemuriformes, Lorisiformes, Tarsiiformes, Platyrrhini, and Catarrhini, and combined with available data (13 other primates, 11 nonprimate placentals, and 2 marsupials). Phylogenetic analyses using maximum likelihood on nucleotides and amino acids robustly support the monophyly of primates, Strepsirrhini, Lemuriformes, Lorisiformes, Anthropoidea, Catarrhini, and Platyrrhini. It is interesting to note that 1) Tarsiidae grouped with Anthropoidea, and the support for this node depends on the molecular characters considered; 2) Cheirogaleidae grouped within Lemuriformes; and 3) Daubentonia was the sister group of all other Lemuriformes. Study of the IRBP evolutionary rate shows a high heterogeneity within placentals and also within primates. Maximum likelihood local molecular clocks were assigned to three clades displaying significantly contrasted evolutionary rates. Paenungulata were shown to evolve 2.5-3 times faster than Perissodactyla and Lemuriformes. Six independent calibration points were used to estimate splitting ages of the main primate clades, and their compatibility was evaluated. Divergence ages were obtained for the following crown groups: 13.8-14.2 MY for Lorisiformes, 26.5-27.2 MY for Lemuroidea, 39.6-40.7 MY for Lemuriformes, 45.4-46.7 MY for Strepsirrhini, and 56.7-58.4 MY for Haplorrhini. The incompatibility between some paleontological and molecular estimates may reflect the incompleteness of the placental fossil record, and/or indicate that the variable IRBP evolutionary rates are not fully accommodated by local molecular clocks.     

Molecular evolutionary dynamics of cytochrome b in strepsirrhine primates: the phylogenetic significance of third-position transversions

DNA sequences of the complete cytochrome b gene are shown to contain robust phylogenetic signal for the strepsirrhine primates (i.e., lemurs and lorises). The phylogeny derived from these data conforms to other molecular studies of strepsirrhine relationships despite the fact that uncorrected nucleotide distances are high for nearly all intrastrepsirrhine comparisons, with most in the 15%-20% range. Cytochrome b sequences support the hypothesis that Malagasy lemuriforms and Afro-Asian lorisiforms each comprise clades that share a sister- group relationship. A study (Adkins and Honeycutt 1994) of the cytochrome c oxidase subunit II (COII) gene placed one Malagasy primate (Daubentonia) at the base of the strepsirrhine clade, thereby suggesting a diphyletic Lemuriformes. The reanalysis of COII third- position transversions, either alone or in combination with cytochrome b third-position transversions, however, yields a tree that is congruent with phylogenetic hypotheses derived from cytochrome b and other genetic data sets.      

Lemuriform origins as viewed from the fossil record

Fossils relevant to lemuriform origins are reviewed. Omanodon seems very close to the other early tooth-combed lemuriforms Karanisia, Wadilemur and Saharagalago, whereas Bugtilemur is rejected from the Lemuriformes. The Djebelemurinae, including Djebelemur and 'Anchomomys' milleri, are considered as stem lemuriforms preceding tooth comb differentiation; they are shown to be very distinct from European adapiforms. With tooth-combed lemuriforms present in Africa around 40 million years ago, and stem lemuriforms without tooth combs present on the same continent around 50-48 million years ago, a reasonable scenario can be proposed: tooth comb differentiation and lemuriform dispersal to Madagascar between 52-40 million years ago. The possible significance of Plesiopithecus for daubentoniid origins is raised. A critique of molecular dates is presented in the light of the fossil record. Azibiids are possibly early African prosimians. The timing of the dispersal of primates to Africa and the problem of strepsirhine origins are briefly examined.     

The road less traveled: Phylogenetic perspectives in primatology

Interest in phylogeny is increasing in many areas of evolutionary biology. One area of evolutionary anthropology that has not yet fully embraced this growth in phylogenetic thinking, however, is the study of primate behavior and ecology.¹ The predominant framework for behavioral studies of primates over the last three decades has been socioecological. The goals have been to identify broad correlations between species' behaviors and current environmental conditions. As such, the socioecological approach has been largely nonhistorical, taking little account of phylogeny. In contrast, phylogenetic approaches view the behavior of contemporary taxa within an explicitly historical framework. Although socioecology has proven extremely productive, there are many reasons to think that research in primatology could be profitably supplemented by a phylogenetic perspective.^2,3     

Phylogeny of Neotropical Monkeys: The Interplay of Morphological, Molecular, and Parasitological Data

Separate independent hypotheses of the phylogenetic relationships among the Platyrrhini monkeys have been produced in a recent past, either based upon morphological or molecular data, but the results are generally conflicting and the phylogeny of the group still is debated. The high host specificity observed among primates and their oxyurid parasites allows to consider the result of a morphologically based cladistic analysis of the pinworms of the Platyrrhini as an estimate of the phylogeny of these monkeys. Using the matrix representation method this “parasite-tree” is combined, using parsimony analysis, with several conflicting molecular or morphological hypothesis of the phylogeny of the host group. The results are discussed with respect to previously published classification, or composite computations of the phylogeny, of the Neotropical monkeys. Comparison of different hypothesis makes apparent several stable groups: (i) the Callithrichidae +Saimiri,(ii) the Atelidae/Alouattidae, (iii) the Pitheciidae, and (iv) the Alouattidae/Atelidae + Pitheciidae. In addition, the parasite and the molecular trees support close relationships betweenCallimicoandCallithrix/Cebuella.The study also makes apparent that the parasite tree generally portrays the results of other studies, both when they are congruous and when they are conflicting. This is interpreted to be additional evidence for close coevolution between the Platyrrhini and their specific pinworms. Because, whatever the combination of data being considered no consensus can be found on the exact position ofAotusandCallicebus,and because it is likely that the earliest radiation of the Platyrrhini could be comparable to an evolutionary burst, which renders identification of homologous characters difficult, it is suggested that, possibly, not enough discriminating tracks of the evolutionary paths have been conserved to allow to resolve this uncertainty in the future.     

An alu-based phylogeny of lemurs (infraorder: lemuriformes)

LEMURS (INFRAORDER: Lemuriformes) are a radiation of strepsirrhine primates endemic to the island of Madagascar. As of 2012, 101 lemur species, divided among five families, have been described. Genetic and morphological evidence indicates all species are descended from a common ancestor that arrived in Madagascar ～55-60 million years ago (mya). Phylogenetic relationships in this species-rich infraorder have been the subject of debate. Here we use Alu elements, a family of primate-specific Short INterspersed Elements (SINEs), to construct a phylogeny of infraorder Lemuriformes. Alu elements are particularly useful SINEs for the purpose of phylogeny reconstruction because they are identical by descent and confounding events between loci are easily resolved by sequencing. The genome of the grey mouse lemur (Microcebus murinus) was computationally assayed for synapomorphic Alu elements. Those that were identified as Lemuriformes-specific were analyzed against other available primate genomes for orthologous sequence in which to design primers for PCR (polymerase chain reaction) verification. A primate phylogenetic panel of 24 species, including 22 lemur species from all five families, was examined for the presence/absence of 138 Alu elements via PCR to establish relationships among species. Of these, 111 were phylogenetically informative. A phylogenetic tree was generated based on the results of this analysis. We demonstrate strong support for the monophyly of Lemuriformes to the exclusion of other primates, with Daubentoniidae, the aye-aye, as the basal lineage within the infraorder. Our results also suggest Lepilemuridae as a sister lineage to Cheirogaleidae, and Indriidae as sister to Lemuridae. Among the Cheirogaleidae, we show strong support for Microcebus and Mirza as sister genera, with Cheirogaleus the sister lineage to both. Our results also support the monophyly of the Lemuridae. Within Lemuridae we place Lemur and Hapalemur together to the exclusion of Eulemur and Varecia, with Varecia the sister lineage to the other three genera.     

Primate Behavioral Ecology: From Ethnography to Ethology and Back

Nonhuman primates occupy a special niche in anthropology because of the comparative insights into humans they provide. Initial anthropological interest in primates targeted the apes for their close phylogenetic relationships with humans, and the semiterrestrial Old World monkeys for their ecological similarities with hominids adapting to life on the ground. From the earliest anecdotal reports of tool use and hunting to more contemporary quantitative analyses of local "cultural" traditions, nonhuman primates have challenged deep-rooted concepts of human uniqueness and redefined the boundaries between us and other animals. Yet, despite the long-standing influence of primate studies in anthropology, approaches to studying primates began diverging from those of earlier ethnographers. Advances in primatology, particularly during the 1990s, have included a much deeper understanding of how ecology, phylogeny, and demography affect behavior. Insights into intraspecific, population-level variation represent an important area of convergence between primatology, other areas of anthropology, and conservation biology. [Keywords: primate behavioral ecology, anthropocentrism, evolutionary theory, systematic methods, biology]     

等位基因杂合子现象及其在系统发育学分析中的研究概述

系统发育研究已是澄清所有进化历史问题的必由之路。选择合适的分子标记以及最大限度地挖掘和利用其所包含的系统发育信息是构建可靠的系统发育树的关键。等位基因杂合子(Intra-individual allele heterozygotes, IIAHs)是核基因内含子作为系统发育研究中的分子标记时常常出现的现象。如何挖掘并利用其中所包含的系统发育信息成为近年来系统发育学的研究热点。文章从此现象的产生、杂合子的分离以及现有的研究方法3个方面详尽概述, 阐述了IIAHs及其在系统发育分析中的最新研究进展。     

Primate phylogeny: molecular evidence from retroposons

In these postgenomic times where aspects of functional genetics and character evolution form a focal point of human-mouse comparative research, primate phylogenetic research gained a widespread interest in evolutionary biology. Nevertheless, it also remains a controversial subject. Despite the surge in available primate sequences and corresponding phylogenetic interpretations, primate origins as well as several branching events in primate divergence are far from settled. The analysis of SINEs - short interspersed elements - as molecular cladistic markers represents a particularly interesting complement to sequence data. The following summarizes and discusses potential applications of this new approach in molecular phylogeny and outlines main results obtained with SINEs in the context of primate evolutionary research. Another molecular cladistic marker linking the tarsier with the anthropoid primates is also presented. This eliminates any possibility of confounding phylogenetic interpretations through lineage sorting phenomena and makes use of a new point of view in settling the phylogenetic relationships of the primate infraorders.     

Intrasexual selection and testis size in strepsirhine primates

The main objective of this study was to investigate two predictionsof sexual selection theory concerning interspecific variationin testis size among strepsirhine primates (Lemuriformes andLorisiformes). First, the unique evolutionary history of lemursprovides an opportunity for an independent test of the predictionsof sperm competition theory regarding the relationship betweenmating system and relative testis size. Second, I examined theevolutionary relationship between the morphological correlatesof pre- and postcopulatory competition (i.e., between sexualdimorphism and testis size) because polygamous lemurs, in contrastto other polygamous primates, lack sexual dimorphism. Basedon measurements from 174 captive strepsirhines from 24 species,I found that multi-male species had significantly larger testesthan pair-living ones, but that they did not differ significantlyfrom solitary species. This result deviates from theoreticalexpectations, but may be the result of yet-unknown heterogeneityin mechanisms of male-male competition in both multi-male andsolitary species. There was no difference in relative testissize between nonmonogamous lemurs and lorises, indicating thatpresumably lower levels of precopulatory competition are notnecessarily compensated by more intense sperm competition. Bodysize and phylogenetic effects were also found to considerablyaffect interspecific variability in testis size. Analyses ofindependent contrasts revealed that evolutionary changes inmating system, testis size, sexual size, and canine dimorphismwere not, or only weakly, associated in this monophyletic groupof primates. Additional comprehensive comparative studies ofsexual dimorphism, testis size, mating system, and copulatorybehavior in these and other taxa are indicated to illuminategeneral patterns and causes of covariation among these traits     

Waiting for Sequences: Morris Goodman,Immunodiffusion Experiments,and the Origins of Molecular Anthropology

During the early 1960s, Morris Goodman used a variety of immunological tests to demonstrate the very close genetic relationships among humans, chimpanzees, and gorillas. Molecular anthropologists often point to this early research as a critical step in establishing their new specialty. Based on his molecular results, Goodman challenged the widely accepted taxonomic classification that separated humans from chimpanzees and gorillas in two separate families. His claim that chimpanzees and gorillas should join humans in family Hominidae sparked a well-known conflict with George Gaylord Simpson, Ernst Mayr, and other prominent evolutionary biologists. Less well known, but equally significant, were a series of disagreements between Goodman and other prominent molecular evolutionists concerning both methodological and theoretical issues. These included qualitative versus quantitative data, the role of natural selection, rates of evolution, and the reality of molecular clocks. These controversies continued throughout Goodman’s career, even as he moved from immunological techniques to protein and DNA sequence analysis. This episode highlights the diversity of methods used by molecular evolutionists and the conflicting conclusions drawn from the data that these methods generated.     

Primate molecular phylogenetics in a genomic era

A primary objective of molecular phylogenetics is to use molecular data to elucidate the evolutionary history of living organisms. Dr. Morris Goodman founded the journal Molecular Phylogenetics and Evolution as a forum where scientists could further our knowledge about the tree of life, and he recognized that the inference of species trees is a first and fundamental step to addressing many important evolutionary questions. In particular, Dr. Goodman was interested in obtaining a complete picture of the primate species tree in order to provide an evolutionary context for the study of human adaptations. A number of recent studies use multi-locus datasets to infer well-resolved and well-supported primate phylogenetic trees using consensus approaches (e.g., supermatrices). It is therefore tempting to assume that we have a complete picture of the primate tree, especially above the species level. However, recent theoretical and empirical work in the field of molecular phylogenetics demonstrates that consensus methods might provide a false sense of support at certain nodes. In this brief review we discuss the current state of primate molecular phylogenetics and highlight the importance of exploring the use of coalescent-based analyses that have the potential to better utilize information contained in multi-locus data.     

Recapitulating the evolution of Afrotheria: 57 genes and rare genomic changes (RGCs) consolidate their history

The decipherment of higher level relationships among the orders of Afrotheria – an extraordinary assumption in mammalian evolution – constitutes one of the major disputes in the evolutionary history of mammals. Recent comprehensive studies of various genomic data, including mitochondrial and nuclear DNA sequences, chromosomal syntenic associations and retroposon insertions support strongly the monophyly of Afrotheria. However, the relationships within Afrotheria have remained ambiguous and there is a necessity for a more sophisticated analysis (i.e. combination of gene phylogeny and Rare Genomic Changes (RGCs)), which could aid in the comprehension of the evolutionary history of this old group of mammals. The present study investigated the phylogenetic relationships within Afrotheria by analysing a data set of coding and non-coding sequences (～32 000 bp) comprising 57 orthologous genes and 31 RGCs, such as chromosomal associations and retroposon insertions, and re-evaluated a molecular timescale for afrotherian mammals using a Bayesian relaxed clock approach. The interordinal afrotherians phylogeny presented here contributed to the elucidation of the evolutionary history of this ancient clade of mammals, which is one of the most unorthodox proposals in mammalian biology. This is critical not only for understanding how Afrotheria evolved in Africa, but also to comprehend the early biogeographical history of placental mammals.     

Phylogenetic relationships among the Malagasy lemuriforms (Primates: Strepsirrhini) as indicated by mitochondrial sequence data from the 12S rRNA gene

Numerous phylogenetic hypotheses have been advanced for the Malagasy lemuriform radiation, drawing on data from morphology, physiology, behaviour and molecular genetics. Almost all possible relationships have been proposed and most nodes have been contested. We present a phylogenetic analysis, using several analytical methods, of a partial sequence from the 12s rRNA mitochondrial gene. This gene codes for the small ribosomal subunit, and functional constraints require that the secondary structure of the molecule is strongly conserved, which in inturn exerts constraints on the primary sequence structure. Although previous studies have suggested a very wide range of phylogenetic applicability for this molecule, our results indicate that it is most useful in strepsirrhine primates for estimating relationships among genera within families and among relatively recently diverged families (mean sequence divergence about 11%). Relationships among families separated by larger genetic distances (>12% divergence; e.g. Cheirogaleidae, Daubentoniidae, Megaladapidae) are difficult to resolve consistently. Our data show strong support for an Indridae-Lemuridae sister group and for monophyly of the Lemuridae with Varecia as the sister to all other lemurids. They also support, albeit less strongly, sister group relationships between Lemur and Hapalemur within the Lemuridae and between PmpLthecus and Avahi in the Indridae.     

Divergence dates for Malagasy lemurs estimated from multiple gene loci: geological and evolutionary context

The lemurs of Madagascar are a unique radiation of primates that show an extraordinary diversity of lifestyles, morphologies and behaviours. However, very little is known about the relative antiquity of lemuriform clades due to the lack of terrestrial fossils for the Tertiary of Madagascar. Here, we employ a Bayesian method to estimate divergence dates within the lemuriform radiation using several unlinked gene loci and multiple fossil calibrations outside the lemuriform clade. Two mitochondrial genes (cytochrome oxidase II and cytochrome b), two nuclear introns (transthyretin intron 1 and von Willebrand factor gene intron 11) and one nuclear exon (interphotoreceptor retinoid binding protein, exon 1) are used in separate and combined analyses. The genes differ in taxon sampling and evolutionary characteristics but produce congruent date estimates. Credibility intervals narrow considerably in combined analyses relative to separate analyses due to the increased amount of data. We also test the relative effects of multiple vs. single calibration points, finding that, when only single calibration points are employed, divergence dates are systematically underestimated. For the mitochondrial DNA data set, we investigate the effects of sampling density within the mouse lemur radiation (genus Microcebus). When only two representative species are included, estimated dates throughout the phylogeny are more recent than with the complete-species sample, with basal nodes less affected than recent nodes. The difference appears to be due to the manner in which priors on node ages are constructed in the two analyses. In nearly all analyses, the age of the lemuriform clade is estimated to be approximately 62-65 Ma, with initial radiation of mouse lemurs and true lemurs (genus Eulemur) occurring approximately 8-12 Ma. The antiquity of the mouse lemur radiation is surprising given the near uniform morphology among species. Moreover, the observation that mouse lemurs and true lemurs are of similar ages suggests discrepancies in rates of morphological, behavioural and physiological evolution in the two clades, particularly with regard to characteristics of sexual signalling. These differences appear to correlate with the nocturnal vs. diurnal lifestyles, respectively, of these two primate groups.     

The phylogenetic placement of Chondrichthyes: inferences from analysis of multiple genes and implications for comparative studies

Elasmobranch fishes (sharks and rays) have proven valuable for inferring general and specific properties of molecular evolution through comparative studies with crown group vertebrates because they are the most ancient group of gnathostomes. Recent studies have questioned the conventional phylogenetic placement of sharks in the vertebrate tree, however. In this paper I review the importance of the basal position of Chondrichthyes for comparative biology and compile evidence from multiple, independent genes to evaluate the phylogenetic placement of sharks. The results suggests that alternative phylogenetic hypotheses of the relationships among the Chondrichthyes, Actinopterygii and Sarcopterygii can not be refuted with available data, implying that the assumption of the basal placement of sharks in the vertebrate tree is suspect. Resolving the phylogeny of basal vertebrates is important for testing hypotheses about the evolution of vertebrates, and the current lack of a robust phylogeny limits evolutionary inferences that can be gained from comparative studies that include sharks and rays.     

Phylogeny, host-parasite relationship and zoogeography

Phylogeny is the evolutionary history of a group or the lineage of organisms and is reconstructed based on morphological, molecular and other characteristics. The genealogical relationship of a group of taxa is often expressed as a phylogenetic tree. The difficulty in categorizing the phylogeny is mainly due to the existence of frequent homoplasies that deceive observers. At the present time, cladistic analysis is believed to be one of the most effective methods of reconstructing a phylogenetic tree. Excellent computer program software for phylogenetic analysis is available. As an example, cladistic analysis was applied for nematode genera of the family Acuariidae, and the phylogenetic tree formed was compared with the system used currently. Nematodes in the genera Nippostrongylus and Heligmonoides were also analyzed, and the validity of the reconstructed phylogenetic trees was observed from a zoogeographical point of view. Some of the theories of parasite evolution were briefly reviewed as well. Coevolution of parasites and humans was discussed with special reference to the evolutionary relationship between Enterobius and primates.     

ORIGINAL ARTICLE: Eyes wide shut: can hypometabolism really explain the primate colonization of Madagascar?

Aim We investigate the hypothesis that it was the capacity for torpor or hibernation that enabled the lemuriforms (and possibly other mammal groups, e.g. tenrecs and rodents) to invade Madagascar by means of over‐water dispersal. Location Madagascar, East Africa and the Mozambique Channel. Methods We consider the body weights and life‐style features of living primate taxa that employ heterothermy. Using this information as a standard for comparison, we summarize the available information on the Palaeogene strepsirrhine radiation (i.e. members of the infraorder Adapiformes, the extinct sister‐taxon to the lemuriforms, as well as putative stem lemuriforms), particularly with respect to possible trends in body weight among early, middle and late Eocene adapiforms. We discuss Eocene climatic conditions in the northern hemisphere and Africa, and assess the likelihood of adaptations for heterothermy in adapiforms. Finally, we estimate the body weights of the common ancestors to the living Lemuriformes and Lemuroidea using the method of phylogenetically independent contrasts. Results The mean body weights estimated for the early, middle and late Eocene strepsirrhine faunas remain at approximately 2 kg, outside of the range of living primates using heterothermy. The adapiforms’ appearance coincided with the ‘initial Eocene thermal maximum’, an unusually hot period of global warming, and their demise corresponded with a major cooling event coincident with the appearance of ice sheets on Antarctica. They show no evidence of having evolved adaptations that allowed them to withstand climatic deterioration. The body weights of the ancestral lemuriform and ancestral lemuroid are of a similar order to the mean body weight estimated for the adapiforms, i.e. approximately 1.8 and 2.1 kg, respectively. Main conclusions The available evidence argues against the widespread use of heterothermy by adapiforms. The adapiform–lemuriform divergence may have been the result of the lemuriforms adapting to the drier and more seasonal environments that characterized the African Eocene, and this suite of adaptations may have included the use of heterothermy, but there is as yet no substantial evidence to confirm the presence of either group on the continent prior to c. 40 Ma. The estimated body weights of the common lemuriform and lemuroid ancestors are well outside the size range of living mammals that employ heterothermy. We conclude that the hypothesis that it was the ability to use heterothermy that enabled the strepsirrhines, and not the haplorhines, to invade Madagascar, is unlikely. Alternative explanations for this anomaly should be sought.