The Journal of Heredity 2001:92(2)
© 2001 The American Genetic Association 92:212-219
Molecular Dating and Biogeography of the Early Placental Mammal Radiation
From the Laboratory of Genomic Diversity, National Cancer Institute, Frederick, MD 21702 (Eizirik, Murphy, and O'Brien) and Department of Biology, University of Maryland, College Park, Maryland (Eizirik). E.E. and W.J.M. contributed equally to this work.
Address correspondence to Eduardo Eizirik at the address above or e-mail: eizirike{at}mail.ncifcrf.gov.
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Abstract |
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The timing and phylogenetic hierarchy of early placental mammal divergences was determined based on combined DNA sequence analysis of 18 gene segments (9779 bp) from 64 species. Using rooted and unrooted phylogenies derived from distinct theoretical approaches, strong support for the divergence of four principal clades of eutherian mammals was achieved. Minimum divergence dates of the earliest nodes in the placental mammal phylogeny were estimated with a quartet-based maximum-likelihood method that accommodates rate variation among lineages using conservative fossil calibrations from nine different nodes in the eutherian tree. These minimum estimates resolve the earliest placental mammal divergence nodes at periods between 64 and 104 million years ago, in essentially every case predating the Cretaceous-Tertiary (K-T) boundary. The pattern and timing of these divergences allow a geographic interpretation of the primary branching events in eutherian history, likely originating in the southern supercontinent Gondwanaland coincident with its breakup into Africa and South America 95–105 million years ago. We propose an integrated genomic, paleontological, and biogeographic hypothesis to account for these earliest splits on the placental mammal family tree and address current discrepancies between fossil and molecular evidence.
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Introduction |
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The phylogenetic pattern and timing of the radiation of eutherian (placental) mammals has been the subject of considerable debate over several decades. Classical and modern analyses based on paleontological data have suggested a rapid adaptive radiation following, and perhaps facilitated by, the extinction of dinosaurs at the Cretaceous-Tertiary (K-T) boundary about 65 million years ago (MYA) (Benton 1999; Bromham et al. 1999; Foote et al. 1999). Recent molecular studies reported genetic divergence estimates that question this view and suggest much earlier dates (74–130 MYA) for the interordinal divergences among placental mammals (Easteal 1999; Hedges et al. 1996; Kumar and Hedges 1998). A pre-K-T boundary differentiation scenario led to the hypothesis that the initial radiation of placental mammals was triggered by vicariant events derived from continental breakup during the Cretaceous (Bromham et al. 1999; Hedges et al. 1996), which may have been enhanced much later by the sudden opening of numerous ecological niches previously occupied by dinosaurs. To distinguish between these two scenarios it is important to consider the variance of molecular dating estimates for early eutherian divergences (e.g., Hedges and Kumar 1999) and to compare results from different approaches and independent data sets. A potentially confounding aspect of molecular dating methods would be rate heterogeneity among lineages, which has been apparent in some studies of placental mammals including rodents (e.g., Gu and Li 1992; Li et al. 1996). A confident interpretation of deep divergence nodes such as those of placental mammals would benefit from explicit tests and adjustment for rate heterogeneity among lineages (Li 1997; Kumar and Hedges 1998; Bromham et al. 2000).
A critical requirement for dating divergence nodes among the earliest placental mammals would be a robust resolution of the phylogenetic topology of the 18 living orders. This information is of direct relevance to designing comprehensive and representative taxon comparisons for molecular dating estimates that span the deepest nodes of Eutheria. Studies using morphological and molecular characters have contributed to the resolution of certain parts of the eutherian tree (e.g., McKenna and Bell 1997; Miyamoto and Goodman 1986; Novacek 1992; Springer et al. 1997), but the structure of the earliest divergences among placentals has remained unclear. Recent molecular data have contributed to resolving these basal nodes (Madsen et al. 2001; Murphy et al. 2001), supporting the existence of four principal clades of placental mammals. Although these studies provide evidence for the placement of the root of the eutherian tree (between clade I [Afrotheria] and the other three clades), we could not exclude two alternative roots (at the base of Xenarthra or between [Afrotheria, Xenarthra] and the other two clades). Moreover, it is possible that the bootstrap support for the basal relationships among the four major clades of placentals was actually decreased by inclusion of the marsupial outgroup, due to its unstable placement (Swofford et al. 1996).
In this article we reexamine the phylogeny, dating, and biogeography of early placental mammals using three approaches: (1) a comparison of the bootstrap support for basal eutherian nodes in extensive rooted versus unrooted phylogenetic analyses of nearly 10,000 aligned nucleotides examined in 64 placental mammal species; (2) a maximum-likelihood-based rate constancy test (quartet dating), which allows for rate heterogeneity among lineages, aiming to specifically test whether the supraordinal divergences within Eutheria preceded the K-T boundary; and (3) an estimation of the dates and 95% confidence intervals for the deep nodes which define the four major clades of eutherian mammals. Using conservative fossil calibrations (which are almost certainly underestimates of true divergence times at those internal nodes) our results support the hypothesis that most, if not all, of the early supraordinal eutherian diversification did precede the K-T boundary (Hedges et al. 1996; Cooper and Penny 1997; Kumar and Hedges 1998). These results, along with current estimates of the position of the eutherian root (Madsen et al. 2001; Murphy et al. 2001), suggest that this early separation of placental lineages was likely the result of vicariant events associated with the breakup of Gondwanaland in the late Cretaceous period.
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Materials and Methods |
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The analyses performed here are based on the dataset presented by Murphy et al. (2001), which consists of 18 gene segments (15 nuclear: ADORA3, ADRB2, APP, ATP7A, BDNF, BMI1, CNR1, CREM, EDG1, PLCB4, PNOC, RAG1, RAG2, TYR, ZFX; and three mitochondrial: 12S rRNA, tRNAVal; partial 16S rRNA; total alignment of 9779 bp) examined in 64 placental mammals, broadly representing all extant orders (Table 1), as well as two marsupial outgroups. The primers used to amplify these segments are listed in Table 2. The use of a long, concatenated data set as opposed to several separate short segments has been suggested to improve the reliability of phylogenetic and dating estimates (Bromhan et al. 2000; Huelsenbeck et al. 1996; Nei et al. 2001).
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Phylogenetic analyses were performed with PAUP*4.0b4a (Swofford 1998) using three optimality criteria: maximum parsimony (MP), minimum evolution with the neighbor-joining algorithm (NJ), and maximum likelihood (ML) using a gamma-corrected HKY85 model with parameters estimated from the dataset (Ts/Tv = 2.0;
= 0.45). Parsimony methods employed heuristic searches (50 replicates, random addition of taxa, TBR branch swapping), and were subdivided into three separate analyses: (1) all sites given equal weight, (2) third codon position transitions removed (CS, conservative substitution parsimony), and (3) transversions weighted two times greater than transitions (2:1 parsimony). Distance analyses employed different distance corrections (Kimura two-parameter, Logdet paralinear, maximum likelihood with an HKY85 model and parameters estimated from the dataset) to examine effects on topological stability. The maximum-likelihood analysis was based on a pruned dataset containing 37 taxa representing all major eutherian lineages. Rooted analyses were performed using two marsupials (representing the neotropical and Australasian lineages, see Table 1) as outgroups, whereas unrooted trees included only eutherian taxa. Bootstrap support was assessed using 1000 replicates for MP and NJ analyses, and 100 iterations for the ML phylogeny. We calculated divergence estimates among placental mammal groups using the quartet dating method (with the program QDate, version 1.11; Cooper and Penny 1997; Rambaut and Bromham 1998) applied to the concatenated dataset of 18 gene segments. This approach involves maximum-likelihood tests of rate constancy in multiple four-taxon trees (quartets), with internal calibration points used for each pair of taxa. In this case we incorporated a two-rate model in which a different rate is allowed for each pair of taxa. Only quartets that did not depart significantly (using a chi-square test) from the expectations of the two-rate model were considered (Rambaut and Bromham 1998). To specifically test whether basal placental lineages diverged prior to the K-T boundary, we calibrated our molecular divergences with conservative dates for the first appearance of nine different mammalian groups in the fossil record. These dates can be considered to be underestimates of true divergence times for these calibration nodes, and therefore our calculations are aimed to be minimum, rather than absolute estimates of basal eutherian divergences.
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Results |
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Our analyses provided consistently high bootstrap support for the four major phylogenetic clades of placental mammals identified by Madsen et al. (2001) and Murphy et al. (2001), as well as for the branch separating Afrotheria + Xenarthra from all other placentals. These results strongly suggest that these basal relationships among eutherians are stable (Figure 2, Table 3), although the ultimate resolution of the early branching order will only be achieved with the firm establishment of the root. We observed that in nearly all cases the bootstrap values for basal branches did increase in the unrooted analyses relative to the rooted trees (Table 3), supporting the prediction that the unstable root was affecting the confidence of ingroup relationships (Swofford et al. 1996).
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The branching pattern observed in Figure 1 shows that the early eutherian radiation was rather rapid (note the short basal internodes coupled with long terminal branches). Furthermore, the observed starlike topology within the supraordinal clades III and IV clearly suggests rapid bursts of diversification within these lineages. Also apparent is the considerable degree of rate variation among placental lineages (Figure 1). Several taxa are clearly accelerated relative to the others, such as the caviomorph rodents (e.g., Cavia, Myocastor), muroid rodents (e.g., Mus, Rattus), hedgehog (Erinaceus), and tenrec (Echinops). These features of the eutherian tree pose a challenge to its complete resolution, but also provide insights into the causative processes and time interval of these events.
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Species included in the pruned dataset for ML analyses. Our current estimate of the placement of the root (Three hundred seventy-seven quartets of taxa covering all major eutherian lineages were tested for rate constancy under a two-rate model (Rambaut and Bromham 1998). We list in Table 4 the 205 of these taxon quartets (54%) that conformed to this model. These quartets that passed this rate constancy test were used to estimate minimum ages of divergence for five basal nodes in the eutherian tree (Table 4). The estimated dates for the early placental mammal divergences range from 64 to 104 MYA (Table 5), consistently older (with one exception, see below) than the K-T boundary. Considerable variance was observed around estimates of the same phylogenetic node, in large part due to the occurrence of outliers associated with particular calibration points (see Table 4). For example, estimates using the caviomorph rodent calibration at 32 MYA consistently resulted in divergence dates much younger than those obtained using other pairs of taxa, perhaps suggesting a more ancient origin for this group. Conversely, estimates using the Cetartiodactyla calibration point tended to produce outlier values that were considerably older than those obtained with other pairs. In spite of these caveats, all of our results strongly support a rapid diversification of the four principal eutherian lineages (I– IV) prior to the K-T boundary, likely 70– 110 MYA (Table 5).
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Discussion |
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The controversy over the timing of early eutherian radiation centers around the discrepancy so far observed between early (Cretaceous) and widely dispersed molecular divergence estimates for extant placental groups, and the abrupt, more recent (post K-T boundary) first fossil appearance of all diagnosable modern lineages of eutherian mammals (Benton 1999; Bromham et al. 1999; Easteal 1999; Foote et al. 1999; Kumar and Hedges 1998). The present results may offer a plausible explanation for this perceived discrepancy and provide evidence for an integrated interpretation of the early steps in the diversification of placental mammals.
The structure of our phylogenetic trees suggests a rather rapid early radiation of eutherians and an extremely fast diversification inside at least two of the major clades (III and IV), which appears to conflict with the more distinctive branching pattern inferred from previous molecular clock estimates (Easteal 1999; Kumar and Hedges 1998). The more spaced pattern observed in previous studies could have been influenced by undetected and therefore uncorrected differences in gene divergence rates among lineages. Bromham et al. (2000) pointed out that currently available rate constancy tests often fail to detect moderate levels of rate heterogeneity, potentially leading to overestimates of divergence dates. Rate heterogeneity may have introduced a bias in the previously reported very old divergence estimates between primates and rodents (Easteal 1990; Kumar and Hedges 1998), and also in the phylogenetic position of rodents in several molecular studies (e.g., Reyes et al. 2000). More recent and extensive molecular analyses (Huchon et al. 2000; Madsen et al. 2001; Murphy et al. 2001) have observed that, with increased taxon sampling and larger nucleotide datasets, rodents are not basal among eutherians, rather they comprise an internal group allied to lagomorphs (cohort Glires), a view consistent with previous inference developed from strong morphological evidence (Novacek 1992). The only other major point of discrepancy derives from Kumar and Hedges' (1998) estimate of the Xenarthra-Primates divergence at about 129 MYA, however, this calculation was based on only three genes and exhibited a large variance (Hedges and Kumar 1999). The remaining estimates provided by Kumar and Hedges (1998) are actually compatible with a rapid diversification of placental mammals and are largely consistent with our results (Table 5). For example, Kumar and Hedges' (1998) estimate of the divergences between Afrotheria versus Primates (105 ± 6.6 MYA), Ferungulata (part of our clade IV) versus Primates (92 ± 1.3 MYA), and within Ferungulata (74 ± 5.7 MYA to 83 ± 4 MYA) clearly overlap with our 95% confidence intervals (Table 5).
Regarding the age of these divergences, the quartet dating analyses indicate minimum dates for the basal eutherian nodes that are almost exclusively pre-K-T boundary (Table 5), thus supporting previous independent molecular studies (Cooper and Penny 1997; Hedges et al. 1996; Kumar and Hedges 1998). Given the observed variance around these estimates, we conclude that even larger datasets will be needed to produce narrower confidence intervals. The accuracy of such estimations will also be improved by the availability of progressively more reliable fossil calibrations. In spite of these limitations, our results strongly indicate that the basal eutherian radiation did occur prior to the K-T boundary (perhaps preceding it by tens of millions of years), although not dispersed over the long period suggested by previous molecular studies.
In the absence of compelling molecular evidence linking the age of the primary placental mammal divergences with the K- T boundary, some authors noted that the timing of placental diversification coincides with that of Cretaceous continental breakup (Hedges et al. 1996; Kumar and Hedges 1998). However, this provocative hypothesis had no phylogenetic pattern of diversification that might correlate with specific geological events during the Cretaceous (but see Springer et al. 1997). The topology and timing reported here provide support for a role of vicariant events in the early diversification of placental mammals and implicate the breakup of the southern supercontinent Gondwanaland in the earliest eutherian divergences. Similar patterns of vicariance (the historical separation of formerly continuous faunas as a result of geographic barriers) have been implicated in the diversification of Gondwanan taxa within several other vertebrate groups, including fishes (Murphy and Collier 1997; Farias et al. 1999), amphibians (Feller and Hedges 1998), and birds (Cooper and Penny 1997; van Tuinen et al. 1998).
If one interprets the known geographic distribution of fossils from the four major groups in the context of the basal positions of the two southern hemisphere clades [Afrotheria (Africa) and Xenarthra (South America)] (Figure 1; see also Madsen et al. 2001; Murphy et al. 2001) and the 70–110 MYA estimated date of the basal divergences (Table 5), the results suggest a southern origin for placental mammals prior to the complete breakup of the southern supercontinent Gondwanaland. Considering our molecular data in light of geological and paleontological evidence, the most probable scenario depicts an ancestral placental radiation occurring in Gondwanaland (possibly Africa) around 95–110 MYA, with some biogeographic event isolating the ancestor of Afrotheria in Africa prior to the isolation of Xenarthra in South America. This must have occurred no later than 95 MYA (possibly as early as 105 MYA), since this is the youngest estimated date for the breakup of Africa and South America (Smith et al. 1994). The progenitors of clades III and IV (Figures 1 and 2) emerged shortly thereafter, and their fossil distribution suggests a general Laurasian (northern continents) origin (Benton 1993; Carrol 1988; Dawson and Krishtalka 1984). Paleogeographic reconstructions indicate that Eurasian continental fragments were in close proximity to northern Africa in the Late Cretaceous (Scotese 2000; Smith et al. 1994), providing a potential corridor for migration to and dispersal through northern continents by the ancestors of clades III and IV.
Two alternative scenarios cannot be statistically rejected by our data (Murphy et al. 2001) given the uncertainty of the exact position of the root. The first is a sister group relationship between Afrotheria and Xenarthra, implying a strict drift-vicariance hypothesis relating to the separation of Africa and South America. Second is a hypothesis depicting Xenarthra as the most basal eutherian lineage, which would be in agreement with current morphological views (McKenna and Bell 1997), and would suggest that the early placental radiation took place in an interval constrained between 105 MYA and 65 MYA.
Two other points can be made that further bridge the discrepancy between fossil and molecular views of the early eutherian radiation. The phylogenetic resolution of four primary clades of placental mammals (Madsen et al. 2001; Murphy et al. 2001; this study) indicates that each clade retains insectivorous species that bear features some believe are primitive for all placentals. This is in agreement with the hypothesis that the earliest lineage-splitting events in eutherian history were decoupled from the subsequent morphological diversification that culminated in extant groups, most likely after the K-T boundary (Easteal 1999; Foote et al. 1999). If those primitive insectivorous lineages became initially isolated by continental breakup, the impressive adaptive radiation leading to modern orders seems to have occurred in parallel in different geographic locations (as suggested by Madsen et al. 2001), and may have been constrained in each of them until diverse ecological niches became available after the abrupt demise of the dinosaurs.
A final consideration is the inferred Gondwanan origin for the major eutherian lineages. This hypothesis may help explain the current lack of recognizable fossils of modern placentals prior to the K-T boundary, since the Late Cretaceous mammalian fossil record of the southern hemisphere continents (particularly Africa) is relatively poorly known (Foote et al. 1999). These findings, inferences, and their biogeographic implications may help resolve some of the previous discrepancies between paleontological and molecular approaches, and will hopefully stimulate further investigation into the plausible origin of all major extant mammal lineages (monotremes, marsupials, and eutherians) in the southern continents.
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Acknowledgments |
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We thank W. E. Johnson, A. L. Roca, M. Dean, and M. Smith (Laboratory of Genomic Diversity), as well as J. Mussel (Johns Hopkins University) for helpful suggestions and discussions, and the Advanced Biomedical Computing Center (NCI-Frederick) for computational assistance. This work was supported by CNPq, Brazil (to E.E.).
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Footnotes |
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Corresponding Editor: Sudhir Kumar
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References |
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H. Jow, C. Hudelot, M. Rattray, and P. G. Higgs Bayesian Phylogenetics Using an RNA Substitution Model Applied to Early Mammalian Evolution Mol. Biol. Evol., September 1, 2002; 19(9): 1591 - 1601. [Abstract] [Full Text] [PDF]
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D. Huchon, O. Madsen, M. J. J. B. Sibbald, K. Ament, M. J. Stanhope, F. Catzeflis, W. W. de Jong, and E. J. P. Douzery Rodent Phylogeny and a Timescale for the Evolution of Glires: Evidence from an Extensive Taxon Sampling Using Three Nuclear Genes Mol. Biol. Evol., July 1, 2002; 19(7): 1053 - 1065. [Abstract] [Full Text] [PDF]
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