Molecular Evidence of Primate Origins and Evolution

Molecular data have become an important source of evidence on primate evolutionary history, particularly when the fossil evidence is limited or lacking. The most recent molecular phylogenetic studies of primate evolutionary relationships and divergence times are reviewed here, primarily at the family level and above. Paleontological data are not entirely omitted, but the focus here is on the molecular results. The current molecular evidence for the branching pattern among the primates, colugos, and treeshrews is presented, and current studies provide weak support for a sister group relationship between primates and colugos. The haplorhine affinities of the tarsier are documented out of a sense of duty; hopefully, it will be possible to stop pretending this is an open question sometime soon. The relationships among the platyrrhine families are quite convincingly resolved in favor of an atelid and cebid clade, but the relationships among Aotus, the cebines, and the callitrichines in the Cebidae are poorly resolved. It seems that the molecular evidence will eventually support reciprocal monophyly of the living galagos and lorises, but the molecular data are not presently very helpful. Excluding the early diverging Daubentonia lineage, the relationship of the remaining four lemur families almost certainly includes a cheirogaleid-lepilemurid clade but is otherwise poorly resolved by molecular data. Advances in divergence date estimation methodology have begun to rectify some of the absurdly early estimates for the time of origin of the crown primate radiation, but there is still a lot of work to do. Fossil calibration remains problematically applied, and some highly cited studies have poorly justified or unjustifiable calibrations. New methods are being developed for mostly or completely fossil calibration-free divergence date estimation and are very promising. Introduction Studies of molecular data have contributed significantly to our understanding of primate origins and evolution, from the seminal immunological studies in the 1960s (Goodman 1961, 1963; Sarich and Wilson 1966, 1967) that contributed to a revision of the hominoid relationships and dramatically shortened the time frame of human evolution to the early years of the DNA era when substantial morphological homoplasy in the Papionini was confirmed from analysis of mitochondrial DNA (mtDNA) sequences (Disotell et al. 1992; Disotell 1994). But what have molecular data done for you lately? In this chapter, the most recent molecular evidence on the higher level relationships of primates is reviewed, from their nearest interordinal relatives to relationships among families and some subfamilies, and presents the most recently published estimates of divergence times. The ideal molecular phylogenetic study of the primates would include unbiased, genome-wide sequence data from all primate species. These data would be analyzed using the best available phylogenetic reconstruction method; if, as is the case 1084 R.L. Raaum today, there were several well-regarded methods, they would be analyzed using all leading approaches. Any significant discrepancy among the results from the different methods would be investigated and explained. To the extent that primate evolution can be represented by a strictly bifurcating history, a single best estimate of the phylogeny would be presented. Lineage divergence dates (with confidence intervals) would be calculated from evolutionary rate estimates along lineages derived from either well-dated, justifiable calibration points or some other independent rate estimate. No such study has been published. Nothing even comes particularly close. It is an impossible ideal at the moment. Aside from the expense and practical problems associated with collecting sequence data from all primate species, or even all genera, it is not clear that current computational abilities could efficiently analyze the data. Given that current efforts must fall short of the ideal, it is necessary to choose the best estimates among studies with various shortcomings. For most primate groups, there are now dozens of published phylogenies and divergence date estimates. Given all these choices, it is possible to support quite different evolutionary scenarios by cherry-picking convenient results. One source of this proliferation is that most research groups with a focus on molecular systematics publish series of papers with expanding datasets and new methods. From these series, only the most recently published are presented, unless there are important differences in dataset, question, or analytic method between successive papers from a single author or research group. In addition, no phylogeny or divergence date study published more than a decade ago is given a great deal of weight; these older papers are usually based on very limited datasets and outmoded methods of analysis. The history of the discipline is, of course, important, but the main goal of this review is to update the reader on the most current molecular evidence on primate origins and evolution. Broader taxon sampling is known to improve phylogenetic reconstruction (Hendy and Penny 1989; Baurain et al. 2007), so the results from studies with broader taxon sampling are prioritized here. However, in the pursuit of the broadest possible taxon sampling, it has become common to create data matrices with large amounts of missing data (e.g., 70 % missing data in Fabre et al. (2009). Whether missing data negatively counteract the benefits of being able to include more taxa is contentious (Misawa and Nei 2003; Lemmon et al. 2009; Simmons 2012; Wiens and Tiu 2012; Roure et al. 2013), and little work has been done on the effect of missing data on divergence date estimation. Studies that report clearly erroneous topologies are excluded. For instance, not only were Arnason et al. (2008) unable to resolve the phylogenetic position of the tarsier, they placed the colugo (flying lemur) as the sister taxon to the anthropoids within the primates. Of course, some relationships are unknown, and it would be unfair to fault a study that reports a relationship that is now rejected if, at the time the study was published, the relationship in question was truly poorly understood. However, in 2008, even if one only read the molecular systematic literature, it was readily apparent that the tarsier is a haplorhine and colugos are not primates (Goodman et al. 1998; Zietkiewicz et al. 1999; Murphy et al. 2001b; Schmitz et al. 2001, 2002; Waddell et al. 2001; Janecka et al. 2007). Molecular Evidence on Primate Origins and Evolution 1085 Admittedly, these criteria are subjective. Therefore, apart from filtering out older studies that have been superseded by more recent publications from the same research groups, studies that are simply outmoded, and publications with dramatically incorrect topologies, data are presented from most broadly sampling primate molecular systematic publications from the last decade. In the figures, those studies that have the best estimates are italicized. In case the reader’s preferences differ, information about all of the included divergence date studies (Table 1) and their calibration points (Table 2) are tabulated so that you may make your own informed choices. Calibration Most current divergence date estimation methods rely on fossil calibration points, but good calibration is hard to achieve (Raaum et al. 2005; Benton et al. 2009). At the very minimum, a fossil securely within the clade must support any calibrated node. For instance, a fossil used to calibrate the minimum age of the ancestor of the living catarrhines must be attributed by a reasonable consensus of primate paleontologists to the crown catarrhines. This seems obvious, but look through recently used calibrations (Table 2). It should be clear by now that any molecular systematist who attempts to estimate divergence dates using fossil calibration points should be conversant enough with the paleontological literature to be able to cite specific fossil taxa or really must seek out some paleontologist colleagues. Fossils can only constrain the most recent age of a clade (Hedges and Kumar 2004; Raaum et al. 2005; Benton et al. 2009). If a fossil is properly identified as the earliest member of a clade, then it is not possible for the common ancestor of that clade to have lived more recently. However, there is nothing that can conclusively and usefully constrain the earliest age of a clade. It is possible to absolutely constrain the ancestor of the living catarrhines to sometime after the earliest evidence for land animals, but this is not useful. Despite this, upper bounds on calibration points are common. This ubiquity exists because most divergence dating algorithms require an upper boundary to provide reasonable estimates. For instance, the popular MCMCTree software requires either at least one lower and one upper bound or a calibration distribution that can act as both upper and lower bound (e.g., a normally distributed calibration prior) (Yang and Rannala 2006). The most commonly used divergence dating algorithms allow the use of probability distributions for calibrations. These probability distributions are an estimate of the likelihood that the true divergence falls within a particular range of dates. For instance, most paleontological data suggests that the most recent common ancestor of humans and chimpanzees lived prior to 5 Ma with no fossils suggestive of common ancestors prior to about 7 Ma. Given these data, it is possible to construct a prior belief (probability distribution) on the likely date of the human-chimpanzee divergence. It is the responsibility of the investigator to ensure that the calibration distribution that is chosen reflects paleontological understanding. For commonly chosen calibration nodes, it might be reasonable to believe that investigators would 1086 R.L. Raaum