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Fossil and Molecular Evidence Constrain Scenarios for the Early Evolutionary and Biogeographic History of Hystricognathous Rodents

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Fossil and Molecular Evidence Constrain Scenarios for the Early Evolutionary and Biogeographic History of Hystricognathous Rodents Fossil and molecular evidence constrain scenarios for the early evolutionary and biogeographic history of hystricognathous rodents Hesham M. Sallama,1, Erik R. Seiffertb, Michael E. Steiperc,d, and Elwyn L. Simonse;1 aDepartment of Earth Sciences, University of Oxford, Parks Road, Oxford OX1 3PR, United Kingdom; bDepartment of Anatomical Sciences, Stony Brook University, Stony Brook, NY 11794; cDepartment of Anthropology, Hunter College of the City University of New York, 695 Park Avenue, NY 10065; dDepartments of Anthropology and Biology, Graduate Center of the City University of New York, 365 Fifth Avenue, NY 10016; and eDivision of Fossil Primates, Duke Lemur Center, 1013 Broad Street, Durham, NC 27705 Contributed by Elwyn L. Simons, Duke Lemur Center, Durham, NC, August 11, 2009 (sent for review July 12, 2009) The early evolutionary and paleobiogeographic history of the diverse Afro-Arabian and South American distributions, respectively, the early rodent clade Hystricognathi, which contains Hystricidae (Old World biogeographic history of crown Hystricognathi remains a matter of porcupines), Caviomorpha (the endemic South American rodents), persistent debate. Some have argued that phiomorphs and caviomorphs and African Phiomorpha (cane rats, dassie rats, and blesmols) is of are likely to have shared a common Afro-Arabian ancestor (15–17), great interest to students of mammalian evolution, but remains while others have suggested that the phiomorph-caviomorph split might poorly understood because of a poor early fossil record. Here we have occurred in Asia, and that caviomorphs dispersed to South describe the oldest well-dated hystricognathous rodents from an America either through Afro-Arabia or via a southern Gondwanan earliest late Eocene (Ϸ37 Ma) fossil locality in the Fayum Depression route (13, 18). One critical issue that has hindered understanding of the of northern Egypt. These taxa exhibit a combination of primitive and group’s historical biogeography is the phylogenetic position of the derived features, the former shared with Asian ‘‘baluchimyine’’ ro- family Hystricidae, which has been placed as either the sister group of dents, and the latter shared with Oligocene phiomorphs and cavi- a phiomorph-caviomorph clade or as the sister group of Caviomorpha, omorphs. Phylogenetic analysis incorporating morphological, tempo- in recent molecular phylogenetic analyses (9, 19–21). Temporal and ral, geographic, and molecular information places the new taxa as tectonic constraints on competing biogeographic hypotheses have also successive sister groups of crown Hystricognathi, and supports an been limited by radically different molecular estimates of the phio- Asian origin for stem Hystricognathi and an Afro-Arabian origin for morph-caviomorph split, which range in age from Ϸ85 Ma to Ϸ36 Ma crown Hystricognathi, stem Hystricidae, and stem Caviomorpha. Mo- (9, 18, 19, 22, 23). lecular dating of early divergences within Hystricognathi, using a Here we present two lines of evidence that help to constrain Bayesian ‘‘relaxed clock’’ approach and multiple fossil calibrations, competing scenarios for the early evolutionary and biogeographic suggests that the split between Hystricidae and the phiomorph- history of Hystricognathi. First, we describe the oldest well-dated caviomorph clade occurred Ϸ39 Ma, and that phiomorphs and cavi- hystricognathous rodents, based on a number of recently recovered omorphs diverged Ϸ36 Ma. These results are remarkably congruent mandibular and maxillary remains and isolated teeth of two recently with our phylogenetic results and the fossil record of hystricogna- discovered species from a Ϸ37 Ma locality in the Fayum Depression. thous rodent evolution in Afro-Arabia and South America. Second, we present independent estimates for the time of origin of crown Hystricognathi, and for the divergence between Caviomorpha Caviomorpha ͉ Eocene ͉ Hystricidae ͉ Oligocene ͉ Phiomorpha and Phiomorpha, employing a Bayesian ‘‘relaxed clock’’ analysis of a recently published molecular dataset that provided strong support for he fossiliferous sedimentary deposits exposed north of Birket the placement of Hystricidae as a sister group of a Phiomorpha- TQarun in the Fayum Depression, northeast Egypt, have produced Caviomorpha clade (24). The fossil and molecular evidence are re- a remarkable collection of fossil mammals from localities that range in markably congruent in suggesting an Afro-Arabian origin of crown age from earliest late Eocene (Ϸ37 Ma, early Priabonian) to latest early Hystricognathi in the late-middle Eocene, and a late Eocene divergence Oligocene (Ϸ29 Ma, late Rupelian) (1–3). Among the more common of Caviomorpha and Phiomorpha. mammals represented in these deposits are primitive members of the Cusp and crest nomenclature follows Wood and Wilson (25) and hystricognathous rodent clade Phiomorpha, now represented by the Marivaux et al. (14) [see supporting information (SI) Fig. S1]. living cane rats (Thryonomyidae), dassie rats (Petromuridae), and blesmols (Bathyergidae). Early Oligocene (i.e., Ϸ33.9–28.5 Ma) phio- Results morphs from Egypt have played a central role in debates surrounding Systematic Paleontology. Placentalia Owen, 1837; Order Rodentia the origin of Hystricognathi (4, 5), a large radiation currently repre- Bowdich, 1821; Infraorder Hystricognathi Tullberg, 1899; Genus sented by 230 extant species; in addition to Phiomorpha, the group also Protophiomys Jaeger et al., 1985. includes the New World Caviomorpha and Old World porcupines of the family Hystricidae (6). Members of Hystricognathi are distinguished Type Species. Protophiomys algeriensis Jaeger et al., 1985. from other rodents by a number of derived anatomical features, most notably the placement of the angular process on the mandible, which is Distribution. Late Eocene of eastern Algeria and northern Egypt situated lateral to the long axis of the lower incisor, rather than in the and possibly Namibia (26). same plane as the lower incisor (as in taxa with ‘‘sciurognathous’’ mandibles) (7). Author contributions: H.M.S., E.R.S., and M.E.S. designed research; H.M.S., E.R.S., M.E.S., The distribution of early fossil phiomorphs and caviomorphs on and E.L.S. performed research; H.M.S., E.R.S., and M.E.S. analyzed data; and H.M.S., E.R.S., isolated southern landmasses during the Paleogene is a longstanding and M.E.S. wrote the paper. paleobiogeographic problem in mammalian evolution (8, 9). The The authors declare no conflict of interest. discovery of hystricognathous tsaganomyid (10) and ‘‘baluchimyine’’ 1To whom correspondence may be addressed. E-mail: [email protected] or (11–13) rodents in Paleogene deposits of Asia has been interpreted as [email protected]. supporting an Asian origin for the stem lineage of Hystricognathi (10, This article contains supporting information online at www.pnas.org/cgi/content/full/ 13, 14), but because early phiomorphs and caviomorphs have strictly 0908702106/DCSupplemental. 16722–16727 ͉ PNAS ͉ September 29, 2009 ͉ vol. 106 ͉ no. 39 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0908702106 Downloaded by guest on September 28, 2021 A BCD E F G HI J K L M N OP Q R S T U V W X Y Fig. 1. Isolated teeth of Protophiomys aegyptensis, sp. nov. (A) DPC 21220G, right DP4;(B) DPC 21385J, right DP4;(C) DPC 21360G, left P4;(D) DPC 21452H, right P4; (E) DPC 21371M, right M1;(F) DPC 21293Q, right M1;(G) DPC 21500N, left M1;(H) DPC 21294H, right M2;(I) CGM 83695, holotype right M2;(J) DPC 21538G, left M2;(K) 2 2 3 3 DPC 21221I, left M ;(L) DPC 21747K, left M ;(M) DPC 21452I, left M ;(N) DPC 21374I, right M ;(O) DPC 21358K, left DP4;(P) DPC 21488I, right M1;(Q) DPC 21747L, right M1;(R) DPC 21538H, left M1;(S) DPC 21374J, left M1;(T) DPC 21296I, right M2;(U) DPC 21221G, right M2;(V) DPC 21360I, right M2;(W) DPC 21294I, right M3;(X) DPC 21365F, right M3;(Y) DPC 21220I, right M3. Emended Diagnosis. Cheek teeth with low cusps and lophs; metaloph Description. DP4 (see Fig. 1 A and B) is a small molariform tooth with joins the metaconule and never connects to the posteroloph; mesolo- crown length greater than width; the lingual margin is narrower than the phule is weakly-developed or nonexistent on the upper cheek teeth; labial margin. The primary cusps are almost equal in height, but the endoloph present on M2–3; metalophulid II is short on lower cheek protocone and hypocone are larger in occlusal view, with crests that are teeth; anterior cingulid is either very weak or absent altogether on lower more obliquely oriented than those on the paracone and metacone. molars. There is no mesolophule. The anteroloph is low and weak and fuses with a small parastyle near the base of the paracone. The metaloph courses lingually from the metacone parallel to the protoloph; it is Protophiomys aegyptensis, New Species. connected to the metaconule via a short and weakly developed crest. A well-developed metaconule is connected to the hypocone via the latter Etymology. Specific epithet is from aegyptos, Greek for Egypt. cusp’s anterior arm. The posteroloph runs labially from the hypocone, 2 coursing around the posterior margin of the tooth, but does not connect Holotype. CGM 83695, an upper right M (Fig. 1I). EVOLUTION to the metacone, leaving a small notch. Isolated P4s attributable to P. aegyptensis demonstrate that the species Type Locality. Birket Qarun Locality 2 (BQ-2), Fayum, Egypt. replaced its DP4 during life, unlike the derived phiomorphs that appear in the same area later in the Paleogene. P4 is roughly triangular in out- Formation and Age. Umm Rigl Member of Birket Qarun Formation, line (Fig. 1 C and D) and smaller than DP4. The paracone and meta- earliest Priabonian in age (Ϸ37 Ma). cone are equal in size and separated by a deep notch. The anteroloph is the weakest and lowest of the 4 transverse lophs. The metaloph and Diagnosis. P. aegyptensis differs from the type species P. algeriensis in the posteroloph connect the metacone to a very small hypocone. The exhibiting the following combination of features: DP4 (Fig.
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