early evolution and biogeography of lorisiform strepsirrhines

American Journal of Primatology 69:27–35 (2007)

RESEARCH ARTICLE

Early Evolution and Biogeography of LorisiformStrepsirrhines

ERIK R. SEIFFERT�

Department of Earth Sciences and Museum of Natural History, University of Oxford,Oxford, United Kingdom

This brief review summarizes new paleontological and molecular datathat together support a late middle Eocene Afro-Arabian origin for crownLorisiformes. Phylogenetic analysis indicates that late Eocene Karanisiais a possible stem lorisiform, late Eocene Saharagalago and Wadilemurand Miocene Komba are stem galagids, and early Miocene Mioeuoticusand Progalago may be crown lorisids. Character evolution along thelorisid and galagid stem lineages is reconstructed as having occurredprimarily in postcranial and dental morphology, respectively. Thesepatterns have important implications for interpreting an early lorisiformfossil record that is still composed primarily of jaws and isolated teeth.Am. J. Primatol. 69:27–35, 2007. �c 2006 Wiley-Liss, Inc.

Key words: Eocene; Miocene; Galagidae; Lorisidae; Lorisiformes

INTRODUCTION

Our understanding of early lorisiform evolution has changed quite radicallysince the turn of the century, thanks to new fossil discoveries that haveunexpectedly doubled the temporal range of crown Lorisiformes [Seiffert et al.,2003], the publication of molecular divergence estimates that are remarkablycongruent with this expanded lorisiform fossil record [Yoder & Yang, 2004], andthe long-awaited identification of molecular markers that have clarified theinterrelationships of extant lorisid genera [Roos et al., 2004]. This review brieflysummarizes these recent developments and discusses the implications of thesedata for our understanding of the origin and historical biogeography of crownlorisiforms.

INTERRELATIONSHIPS OF EXTANT LORISIFORMS

Morphological and genetic data have consistently supported a monophyleticGalagidae, but the molecular evidence for lorisid monophyly has long beenunstable, with immunodiffusion and nucleotide data tending to support the

Published online in Wiley InterScience (www.interscience.wiley.com).DOI 10.1002/ajp.20324

Received 7 July 2005; revised 6 February 2006; revision accepted 15 February 2006

�Correspondence to: Erik R. Seiffert, Department of Earth Sciences and Museum of NaturalHistory, University of Oxford, Parks Road, Oxford OX1 3PR, UK.E-mail: [email protected]

rr 2006 Wiley-Liss, Inc.

paraphyly of lorises with respect to galagos [Dene et al., 1976; Goodman, 1967;Goodman et al., 1998; Masters et al., 2005; Porter et al., 1997; Poux & Douzery2004; Roos et al., 2004; Sarich & Cronin 1976; Yoder et al., 2001], despite animpressive array of postcranial morphological specializations that appear to uniteLorisidae as a well-defined clade [Gebo, 1989; Rasmussen & Nekaris, 1998; Yoderet al., 2001]. Possible resolution of this conflict between molecular andmorphological data has been only recently provided by Roos et al. [2004], whodetected a number of Alu short interspersed nuclear elements (SINEs) thatsolidify support for the existence of African (Arctocebus-Perodicticus) and Asian(Loris-Nycticebus) clades within a monophyletic Lorisidae. Unlike the nucleotidecharacters that were previously used to estimate lorisiform phylogeny, SINEsshould, in the absence of incomplete lineage sorting, be essentially immune tohomoplasy and reversal [Shedlock et al., 2000]. The interrelationships of extantgalagid genera remain controversial [Masters & Brothers, 2002], and unfortu-nately no SINEs have been detected that could convincingly resolve theinterrelationships of Galago, Galagoides, and Otolemur. However, Roos et al.’s[2004] analysis of the mitochondrial locus cytochrome b has provided compellingsupport for a Galago-Otolemur clade to the exclusion of Galagoides, and thisresult is in general agreement with DelPero et al. [2000] and Yoder et al.’s [2001]analyses of the same locus, as well as DelPero et al.’s [2000] analyses of two othermtDNA loci (12S and 16S rRNA) and Yoder et al.’s [2001] analysis of the nuclearIRBP gene.

FOSSIL AND MOLECULAR EVIDENCE FOR THE ANTIQUITYOF CROWN LORISIFORMS

The fossil record documenting early lorisiform evolution has long been asource of great interest for paleoprimatologists, largely because Tertiary lorisi-forms have, for many decades, been the oldest representatives of the entire crownstrepsirrhine radiation. Recent paleontological work in Egypt has significantlyexpanded the temporal range of fossil lorisiforms and crown strepsirrhineswith the recovery of a �37-million-year-old (Ma) stem galagid (Saharagalago)and a loris-like strepsirrhine (Karanisia) whose dental morphology resemblesthat of the extant lorisid Arctocebus [Seiffert et al., 2003]. These taxa areapproximately twice as old as the oldest Miocene lorisiforms from east Africa, andsuggest that crown Lorisiformes had appeared by at least the late middle Eocene.This hypothesis gains additional support from recently recovered dental remainsof the �34 Ma species Wadilemur elegans, which was previously thought to be ananchomomyin adapiform [Simons, 1997]. These specimens indicate that thatspecies is also likely to be a primitive stem galagid [Seiffert et al., 2005b].A proximal femur of W. elegans is also clearly galagid-like and bears greatestsimilarity to the early Miocene stem galagid Komba, although the polarities of theproximal femoral characters that Wadilemur shares with younger galagids arecurrently unclear. Bayesian analyses of nuclear and mitochondrial nucleotidesequences have independently recovered congruent middle Eocene estimates forthe origin of crown Lorisiformes [Yang & Yoder, 2003; Yoder & Yang, 2004],although some other divergence estimates within crown Strepsirrhini indicate amuch later (early or middle Miocene) origin for crown lorisiforms [Porter et al.,1997; Poux & Douzery, 2004].

Phylogenetic analysis of morphological data supports a stem galagidplacement for Saharagalago and Wadilemur, but the position of Karanisia isunstable (Fig. 1a and c) [Seiffert et al., 2005b]. With increased taxon and

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Am. J. Primatol. DOI 10.1002/ajp

character sampling, and the constraint of Arctocebus-Perodicticus monophyly,Karanisia is placed as either a stem lorisiform (Fig. 1a) or a crown strepsirrhine ofuncertain affinities (Fig. 1b), given different treatments of certain multistatecharacters. In light of these results, it appears increasingly likely that theArctocebus-Karanisia clade recovered by Seiffert et al. [2003] was based onhomoplasious and/or plesiomorphic features of the upper and lower dentition, andthat Karanisia is not a crown lorisid.

MIOCENE LORISIFORMS AND CHARACTER EVOLUTION

Although numerous studies have focused on the early Miocene east Africanlorisiforms Komba, Mioeuoticus, and Progalago [Gebo, 1986, 1989; Le Gros Clark,1956; Le Gros Clark & Thomas, 1952; Leakey, 1962; MacInnes, 1943; McCrossin,1992; Phillips & Walker, 2002; Simpson, 1967; Szalay & Katz, 1973; Walker, 1970,1974, 1978], specialists have never reached a consensus as to whether these taxaare stem or crown members of Galagidae and Lorisidae [McCrossin, 1992; Phillips& Walker, 2002], or possibly advanced stem, or very basal crown, lorisiforms[Rasmussen & Nekaris, 1998]. When Mioeuoticus bishopi and Progalagosonghorensis are scored for craniodental features and added to the matrix ofSeiffert et al. [2005a], these species are either nested within Lorisidae [cf.,McCrossin, 1992] or placed as crown lorisiforms of uncertain affinities [cf.,

Fig. 1. A: Relationships among living and extinct crown strepsirrhines, based on a strict consensusof 18 most parsimonious trees (MPTs) recovered from a parsimony analysis with the Miocenelorisiforms Progalago songhorensis and Mioeuoticus bishopi added to Seiffert et al.’s [2005a] matrixof 106 taxa and 360 morphological features (with some multistate characters ordered and scaled).The poorly known adapiform Europolemur dunaifi, which was included in Seiffert et al.’s [2005a]analysis, was excluded from this analysis. Methods are as described in Seiffert et al. [2005a]. Branchcolor/shading reflects biogeographic history, as optimized in Mesquite v. 1.06 [Maddison &Maddison, 2005]. B: Proportion of dental, postcranial, and cranial characters unequivocally andequivocally optimized (ACCTRAN) as having evolved along the lorisiform, lorisid, and galagid stemlineages in the phylogram depicted in A. C: Adams consensus of 1,160‘MPTs, derived from analysisof the Seiffert et al. [2005a] matrix with all characters unordered. D: The same as B, withoptimizations derived from the tree in C.

Early Lorisiform Evolution / 29


Rasmussen & Nekaris, 1998], depending on the treatment of certain multistatecharacters. Regardless of where Mioeuoticus and Progalago are placed,morphological evolution along the galagid and lorisid stem lineages is recon-structed as having occurred primarily in dental and postcranial morphology,respectively (Fig. 1b and d). This pattern implies that stem galagids should beeasy to identify from the most common elements in the primate fossil record (i.e.,mandibles, maxillae, and isolated teeth); however, as it is unlikely that the dentalmorphology of the ancestral crown lorisid differed much from that of theancestral crown lorisiform, it appears that advanced stem lorisiforms, stemlorisids, and extinct crown lorisids may be much more difficult to place as such onthe basis of dental morphology alone.

The absence of clear dental morphological support for the monophyly ofcrown Lorisidae provides some explanation for why the phylogenetic positions ofthe possible lorisids Mioeuoticus and Progalago are so unstable, since both generahave very loris-like teeth and lack the dental synapomorphies of Galagidae, butare not yet clearly represented by postcranial remains. Unfortunately, body massestimates for Mioeuoticus, Progalago, and larger species of Komba show broadoverlap, so it is not possible to confidently assign isolated postcranial elements toany early Miocene species, other than the tiny stem galagid Komba minor.Previous allocations of postcrania to Progalago dorae [Gebo 1989] on the basis ofsize may be incorrect because the galagid-like upper dentitions that have beenattributed to P. dorae actually do not convincingly occlude with the very lorisid-like holotype mandible (containing p4 and m2). If these upper and lowerdentitions are not from the same species, then 1) P. dorae may actually be arelatively rare lorisid, 2) an additional unnamed stem galagid species of similarbody size was present in the east African early Miocene (represented by the‘‘P. dorae’’ upper teeth), and 3) the larger galagid-like postcrania previouslyassigned to P. dorae on the basis of size [Gebo, 1989] may actually belong to thatunnamed galagid species. This hypothesis is supported by the fact that mostpostcranial remains from the early Miocene resemble those that can beconfidently attributed to the tiny stem galagid species Komba minor, and arethus most likely to be attributable to the stem galagids Komba robustus and thegalagid species represented by the ‘‘P. dorae’’ upper teeth.

On temporal grounds, it is unlikely that Mioeuoticus and Progalago areeither stem lorisiforms or very primitive stem galagids, since either placementwould require that these two lineages had independently persisted for 420 Mathrough the later Eocene and Oligocene into the early Miocene, while stem andcrown lorisid lineages that also would have existed during this interval wouldbe completely unsampled. The absence of loris-like postcrania attributable toMioeuoticus or Progalago could simply be due to the fact that these species arevery rare; alternatively, it could be the case that the unique postcranial featuresshared by the African and Asian lorisids evolved in parallel in the two clades[Walker, 1970], and that stem members of these African and Asian clades moreclosely resembled primitive galagids in their postcranial morphology. The shortinternal branch separating the origin of crown Lorisiformes and crown Lorisidae[Roos et al., 2004] certainly leaves little time for all of the shared postcranialadaptations of extant lorises to have evolved. Nevertheless, a maximum-likelihoodestimate for the ancestral mode of locomotion of crown Lorisidae, taking intoaccount three locomotor character states and Roos et al.’s [2004] divergence dateswithin Lorisiformes (Fig. 2), indicates that the ancestral crown lorisid is likely tohave been a slow climber, while the ancestral crown lorisiform is only slightlymore likely to have been a pronograde quadruped than a slow climber. The fact

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that the proximal femoral morphology of �34 Ma Wadilemur is very similar tothat of Komba, and lacks the distinctive features of lorisids [Seiffert et al., 2005b],lends additional support to the hypothesis that the ancestral crown lorisiform wasmore likely to have been a pronograde quadruped (probably with some capacityfor leaping) than a slow climber. The eventual recovery of additional postcranialremains of later Paleogene lorisiforms should help to better characterize thelocomotor adaptations of the ancestral crown lorisiform, and further informthe likelihood that lorisids’ postcranial specializations evolved either in a shortburst along the short internal branch uniting crown lorisids, or in parallel in theAfrican and Asian clades.

STREPSIRRHINE AND LORISIFORM BIOGEOGRAPHY

It has recently been hypothesized that primates originated on the Indo-Malagasy land mass in the late Cretaceous [Marivaux et al., 2001; Martin, 2000,

Fig. 2. Maximum-likelihood optimization of locomotor style within Strepsirrhini, taking intoaccount the divergence dates of Roos et al. [2004] and locomotor categories of Shapiro and Simons[2002]. Pie charts depict the proportional likelihoods for each of the locomotor styles, calculatedin Mesquite v. 1.06 [Maddison & Maddison, 2005].



2003], and that lorisiforms dispersed into Asia, and then Africa, following thecollision of Indo-Pakistan with Asia near the Paleocene-Eocene boundary about55 million years ago. While this scenario would provide a convenient explanationfor the sudden appearance of probable crown primates on northern continents inthe earliest Eocene, it must be emphasized that there is no fossil evidence for thishypothesis. Furthermore, this scenario is very difficult to reconcile with the fossilrecord of crown primates’ closest relatives, such as plesiadapiforms and Glires(the rodent-lagomorph clade), which make their first appearances on northerncontinents in the earliest Paleocene [Clemens, 2004; Johnston & Fox, 1984;Meng, 2004], about 10 million years before Indo-Pakistan collided with Asia. Thefirst undoubted records of other close primate relatives, such as Scandentia (treeshrews) and Dermoptera (flying lemurs), are found in Asia [Ducrocq et al., 1992;Tong, 1988] and support an Asian origin for Primates and stem Strepsirrhini[Beard, 1998], as does the Asian stem primate Altanius, which may be latePaleocene in age [Bowen et al., 2002] and as such could predate the India-Asiacollision. The optimization of a biogeographic character onto topologies derived fromthe phylogenetic analyses presented here suggests either an Asian or Europeanorigin for crown primates, and a European origin for stem Strepsirrhini. The onlypossible crown strepsirrhine from the Asian Paleogene, early Oligocene Bugtilemur,is unlikely to be a cheirogaleid lemuriform as originally claimed [Marivaux et al.,2001], and is probably a primitive relative of the recently described older Asiangenus Muangthanhinius [Marivaux et al., 2006] and the younger North Americanprimate Ekgmowechashala (unpublished results), neither of which had a tooth-comb. Thus, there is no fossil evidence for crown strepsirrhines in Asia until themiddle Miocene, with the first appearance of Nycticeboides [MacPhee & Jacobs,1986] 40 million years after the India-Asia collision, and over 20 million years afterthe first appearance of Saharagalago and Karanisia in Africa.

In this regard it is important that recent phylogenetic analyses of Paleogeneprimates [Seiffert et al., 2005a,b] have recovered two Afro-Arabian lineages–Plesiopithecidae and a Djebelemur-‘‘Anchomomys’’ milleri clade–as successivesister taxa of crown Strepsirrhini to the exclusion of all other Laurasianadapiforms (Fig. 1a and c). These results, combined with Karanisia’s position aseither a stem lorisiform or a crown strepsirrhine of uncertain affinities, appear tobear decisively on the longstanding debate surrounding the geographic origin ofstem and crown lorisiforms [MacPhee & Jacobs 1986; Yoder, 1997]. The simplestbiogeographic explanation for this phylogenetic pattern, with three of the knowncrown lorisiform sister taxa being Afro-Arabian, and the other Malagasy, isclearly an endemic Afro-Arabian origin for both crown Strepsirrhini and crownLorisiformes (Figs. 1a and c, and 3). Interestingly, the optimization of abiogeographic character onto the two topologies derived from the phylogeneticanalyses presented here congruently suggests that the most ancient Afro-Arabianstem strepsirrhine population that ultimately gave rise to crown Strepsirrhiniwas probably derived from a European immigrant. Mean Bayesian estimates ofdivergence dates suggest that this dispersal could have occurred as early as thevery latest Cretaceous [Yoder & Yang, 2004] or as late as the middle Paleocene[Eizirik et al., 2004]. The primate Altiatlasius is known from the late Paleocene ofAfrica (Morocco), and shares some upper molar features with the strepsirrhinesPlesiopithecus and Karanisia (e.g., complete lingual cingula), but on the basis ofavailable evidence Altiatlasius is most likely to be a basal anthropoid [Beard,1998; Godinot, 1994; Seiffert et al., 2005a]. The stem anthropoid placement ofAltiatlasius in the phylogeny figured by Seiffert et al., [2005a], nested alongsideAsian taxa such as eosimiids and living and extinct tarsiers, nevertheless suggests

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that limited primate dispersal between Afro-Arabia and Asia was possible in thePaleocene, notably before the India-Asia collision, and at a time when, themammalian fossil record in Afro-Arabia and Asia for this period of time is poorlysampled. The African stem strepsirrhine Djebelemur may be as old as earlyEocene in age [Hartenberger et al., 1997], and by that time already shows anumber of important morphological differences from Laurasian primates,suggesting a considerable period of endemic evolution on the Afro-Arabian landmass. Paleontological exploration in the Paleocene and early-middle Eocene ofAfro-Arabia should help to further illuminate the nature of crown strepsirrhineorigins and the earliest phases of stem lorisiform evolution.

ACKNOWLEDGMENTS

I thank C. Beard, P. Chatrath, L. Gordon, G. Gunnell, P. Jenkins, R. Kay,B. Marandat, L. Marivaux, E. Simons, and particularly A. Walker for providingaccess to fossils, casts, and/or skeletal material; M. Silcox and two anonymousreviewers for their helpful comments; and A. Burrows and L. Nash for inviting meto participate in the AAPA symposium on ‘‘Evolution, Functional Morphology,and Behavioral Ecology of Lorises and Galagos (Lorisoids).’’

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early evolution and biogeography of lorisiform strepsirrhines

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