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Proc Natl Acad Sci U S A. Sep 29, 2009; 106(39): 16722–16727.
Published online Sep 15, 2009. doi:  10.1073/pnas.0908702106
PMCID: PMC2757825
Evolution

Fossil and molecular evidence constrain scenarios for the early evolutionary and biogeographic history of hystricognathous rodents

Abstract

The early evolutionary and paleobiogeographic history of the diverse rodent clade Hystricognathi, which contains Hystricidae (Old World porcupines), Caviomorpha (the endemic South American rodents), and African Phiomorpha (cane rats, dassie rats, and blesmols) is of great interest to students of mammalian evolution, but remains poorly understood because of a poor early fossil record. Here we describe the oldest well-dated hystricognathous rodents from an earliest late Eocene (≈37 Ma) fossil locality in the Fayum Depression of northern Egypt. These taxa exhibit a combination of primitive and derived features, the former shared with Asian “baluchimyine” rodents, and the latter shared with Oligocene phiomorphs and caviomorphs. Phylogenetic analysis incorporating morphological, temporal, geographic, and molecular information places the new taxa as successive sister groups of crown Hystricognathi, and supports an Asian origin for stem Hystricognathi and an Afro-Arabian origin for crown Hystricognathi, stem Hystricidae, and stem Caviomorpha. Molecular dating of early divergences within Hystricognathi, using a Bayesian “relaxed clock” approach and multiple fossil calibrations, suggests that the split between Hystricidae and the phiomorph-caviomorph clade occurred ≈39 Ma, and that phiomorphs and caviomorphs diverged ≈36 Ma. These results are remarkably congruent with our phylogenetic results and the fossil record of hystricognathous rodent evolution in Afro-Arabia and South America.

Keywords: Caviomorpha, Eocene, Hystricidae, Oligocene, Phiomorpha

The fossiliferous sedimentary deposits exposed north of Birket Qarun in the Fayum Depression, northeast Egypt, have produced a remarkable collection of fossil mammals from localities that range in age from earliest late Eocene (≈37 Ma, early Priabonian) to latest early Oligocene (≈29 Ma, late Rupelian) (13). Among the more common mammals represented in these deposits are primitive members of the hystricognathous rodent clade Phiomorpha, now represented by the living cane rats (Thryonomyidae), dassie rats (Petromuridae), and blesmols (Bathyergidae). Early Oligocene (i.e., ≈33.9–28.5 Ma) phiomorphs from Egypt have played a central role in debates surrounding the origin of Hystricognathi (4, 5), a large radiation currently represented by 230 extant species; in addition to Phiomorpha, the group also includes the New World Caviomorpha and Old World porcupines of the family Hystricidae (6). Members of Hystricognathi are distinguished from other rodents by a number of derived anatomical features, most notably the placement of the angular process on the mandible, which is situated lateral to the long axis of the lower incisor, rather than in the same plane as the lower incisor (as in taxa with “sciurognathous” mandibles) (7).

The distribution of early fossil phiomorphs and caviomorphs on isolated southern landmasses during the Paleogene is a longstanding paleobiogeographic problem in mammalian evolution (8, 9). The discovery of hystricognathous tsaganomyid (10) and “baluchimyine” (1113) rodents in Paleogene deposits of Asia has been interpreted as supporting an Asian origin for the stem lineage of Hystricognathi (10, 13, 14), but because early phiomorphs and caviomorphs have strictly Afro-Arabian and South American distributions, respectively, the early biogeographic history of crown Hystricognathi remains a matter of persistent debate. Some have argued that phiomorphs and caviomorphs are likely to have shared a common Afro-Arabian ancestor (1517), while others have suggested that the phiomorph-caviomorph split might have occurred in Asia, and that caviomorphs dispersed to South America either through Afro-Arabia or via a southern Gondwanan route (13, 18). One critical issue that has hindered understanding of the group's historical biogeography is the phylogenetic position of the family Hystricidae, which has been placed as either the sister group of a phiomorph-caviomorph clade or as the sister group of Caviomorpha, in recent molecular phylogenetic analyses (9, 1921). Temporal and tectonic constraints on competing biogeographic hypotheses have also been limited by radically different molecular estimates of the phiomorph-caviomorph split, which range in age from ≈85 Ma to ≈36 Ma (9, 18, 19, 22, 23).

Here we present two lines of evidence that help to constrain competing scenarios for the early evolutionary and biogeographic history of Hystricognathi. First, we describe the oldest well-dated hystricognathous rodents, based on a number of recently recovered mandibular and maxillary remains and isolated teeth of two recently discovered species from a ≈37 Ma locality in the Fayum Depression. Second, we present independent estimates for the time of origin of crown Hystricognathi, and for the divergence between Caviomorpha and Phiomorpha, employing a Bayesian “relaxed clock” analysis of a recently published molecular dataset that provided strong support for the placement of Hystricidae as a sister group of a Phiomorpha-Caviomorpha clade (24). The fossil and molecular evidence are remarkably congruent in suggesting an Afro-Arabian origin of crown Hystricognathi in the late-middle Eocene, and a late Eocene divergence of Caviomorpha and Phiomorpha.

Cusp and crest nomenclature follows Wood and Wilson (25) and Marivaux et al. (14) [see supporting information (SI) Fig. S1].

Results

Systematic Paleontology.

Placentalia Owen, 1837; Order Rodentia Bowdich, 1821; Infraorder Hystricognathi Tullberg, 1899; Genus Protophiomys Jaeger et al., 1985.

Type Species.

Protophiomys algeriensis Jaeger et al., 1985.

Distribution.

Late Eocene of eastern Algeria and northern Egypt and possibly Namibia (26).

Emended Diagnosis.

Cheek teeth with low cusps and lophs; metaloph joins the metaconule and never connects to the posteroloph; mesolophule is weakly-developed or nonexistent on the upper cheek teeth; endoloph present on M2–3; metalophulid II is short on lower cheek teeth; anterior cingulid is either very weak or absent altogether on lower molars.

Protophiomys aegyptensis, New Species.

Etymology.

Specific epithet is from aegyptos, Greek for Egypt.

Holotype.

CGM 83695, an upper right M2 (Fig. 1I).

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, ...

Type Locality.

Birket Qarun Locality 2 (BQ-2), Fayum, Egypt.

Formation and Age.

Umm Rigl Member of Birket Qarun Formation, earliest Priabonian in age (≈37 Ma).

Diagnosis.

P. aegyptensis differs from the type species P. algeriensis in exhibiting the following combination of features: DP4 (Fig. 1 A and B) lacks a complete endoloph and does not bear an x-shaped pattern of crests around the metaconule; cheek teeth all larger in size (see Table S1); central basin of upper cheek teeth (Fig. 1 E–N) is open labially via a narrow notch; mesolophule is weak and variably reaches the labial wall, connecting with the mesostyle of M2; lower cheek teeth have a relatively short metalophulid II that never reaches the midline of the tooth and is oriented toward either the lingual wall or the metaconid; DP4 is relatively long and narrow, with a longer anterior basin, a metaconid that is placed transverse to the protoconid, a complete posterior arm of the protoconid, and a well-developed anterior arm of the protoconid with an anteroconid; M1 differs in having a strong metalophulid I that connects the metaconid with the protoconid, and in having a very weak anterocingulid; a notch is present between a long posterior arm of the metaconid and the entoconid on the lingual wall; ectostylid is present; posterior basin is long and has a relatively low posterolophid that weakly connects with the entoconid on M3.

Description.

DP4 (see Fig. 1 A and B) is a small molariform tooth with crown length greater than width; the lingual margin is narrower than the labial margin. The primary cusps are almost equal in height, but the protocone and hypocone are larger in occlusal view, with crests that are more obliquely oriented than those on the paracone and metacone. 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 connected to the metaconule via a short and weakly developed crest. A well-developed metaconule is connected to the hypocone via the latter cusp's anterior arm. The posteroloph runs labially from the hypocone, coursing around the posterior margin of the tooth, but does not connect to the metacone, leaving a small notch.

Isolated P4s attributable to P. aegyptensis demonstrate that the species replaced its DP4 during life, unlike the derived phiomorphs that appear in the same area later in the Paleogene. P4 is roughly triangular in outline (Fig. 1 C and D) and smaller than DP4. The paracone and metacone 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 the posteroloph connect the metacone to a very small hypocone. The protocone is connected to the small hypocone by an endoloph.

M1 (see Fig. 1 E–G) is roughly square in shape and bears 4 primary cusps, as well as a small, centrally placed metaconule. The hypocone is directly distal to the protocone and connects to the metaconule via a long anterior arm. The labial wall bears a deep notch between the posterior arm of the paracone and the anterior arm of the metacone; a small mesostyle is variably present. The anteroloph runs parallel to the protoloph to connect to the mesial base of the paracone; a small parastyle is present. The M1 lacks an endoloph, and the lingual sinus is continuous with the central basin. The curved metaloph runs lingually and then mesially to connect to the metaconule and is never oriented distally toward the posteroloph. The mesolophule and mure are either very weak or absent altogether.

M2 (see Fig. 1 H–L) is the largest upper cheek tooth. Overall it is very similar to M1, but differs in having a relatively reduced and more labially situated hypocone, a taller and more curved anteroloph, an endoloph that reaches the anterior arm of the hypocone (closing the lingual side of the central basin), greater development of the mure (although that crest never reaches the protoloph), a weak and interrupted mesolophule that variably reaches the mesostyle on the labial wall, a more narrow labial notch, and a relatively short and low posteroloph that is connected to the base of the metacone.

M3 (see Fig. 1 M and N) is heart-shaped and is the smallest upper molar. It differs from M1–2 in having a reduced metacone and hypocone, the latter of which is labially positioned. A weak mure reaches the midline of the protoloph. An obliquely oriented metaloph courses from the lingual side of the metacone and connects to the metaconule. There is no mesolophule, and the endoloph is low.

The P4 of P. aegyptensis is not yet known. The DP4 (Fig. 1O) has a broad talonid and a narrow trigonid. The “anterolophid” runs from the anterior side of the protoconid toward the mesial side of the metaconid and terminates mesiolabial to the metaconid, leaving a wide notch in the anterior wall of the anterior basin. The metaconid is placed transverse to the protoconid, and a similarly transversely oriented posterior arm of the protoconid joins these cusps. A well-developed anterior arm of the hypoconid attaches to the hypolophid near that crest's junction with the ectolophid. A short mesolophid protrudes from a weak mesoconid. The posterior arm of the metaconid occupies most of the area between the metaconid and entoconid, and there is a wide notch in the lingual wall. A well-developed hypoconulid is present. The posterior basin is open lingually. The labial sinus is wide and deep and bears a worn ectostylid.

The M1 (Fig. 1 P–S) is rectangular in outline and has 5 major cusps. The mesial part of the tooth is narrower than the distal part. A very weak and low anterocingulid runs parallel to the metalophulid I, which is medially interrupted in some individuals. The metalophulid II is short and never reaches the midline of the tooth. The posterior arm of the metaconid forms most of the lingual wall and is interrupted by a narrow notch at the base, where a very short anterior arm of the entoconid is present. A mesostylid is variably present. The posterolophid does not connect to the entoconid, and the transverse hypolophid runs labially from the entoconid to the confluence of the ectolophid and anterior arm of the hypoconid. In the labial sinusid there is a well-developed ectostylid. The hypoconulid is distinct, and a low, poorly developed postcingulid runs labially from that cusp.

The M2 (Fig. 1 T–V) is generally similar to M1, but differs in having trigonids and talonids of almost equal width, and a well-developed mesostylid at the end of the posterior arm of the metaconid. An incipient anterocingulid is present on the M2 of one individual (Fig. 2T). The M3 (Fig. 1 W–Y) is the longest lower molar. The metaconid is tall and mesially situated and the distal part of the crown is relatively long and narrow. The hypoconulid is submerged into the posterolophid and the ectostylid is relatively small.

Fig. 2.
Mandibles, maxillae, and isolated teeth of Waslamys attiai, gen. et sp. nov. (A) DPC 21360H, right DP4; (B) 21365E, right DP4; (C) 21296K, right P4; (D) DPC 21294G, left M1; (E) DPC 21452K, left M1; (F) 21221H, right M2; (G) DPC 21296B, left M2; (H) DPC ...

Waslamys, New Genus.

Type Species.

Waslamys attiai, New Species.

Etymology.

Combination of wasla, Arabic for “joint, junction, or connection,” in reference to the combination of dental features seen in later African phiomorphs and Asian baluchimyines, and mys, Greek for mouse.

Generic Diagnosis.

As for the type species.

Waslamys attiai, New Species.

Etymology.

In honor of the late Yousry Attia, for his important contributions to the study of vertebrate paleontology in Egypt.

Holotype.

CGM 83690, a right maxilla with P4–M3.

Type Locality.

Birket Qarun Locality 2 (BQ-2), Fayum, Egypt.

Formation and Age.

Umm Rigl Member of Birket Qarun Formation, earliest Priabonian in age (≈37 Ma).

Diagnosis.

Waslamys is similar to P. aegyptensis but differs in having a relatively well-developed labial wall (formed by the posterior arm of the paracone and the anterior arm of the metacone) on P4–M3; a relatively well-developed mesolophule on the upper molars; an M1 metaloph that varies between being posteriorly oriented and terminating on the posteroloph, or coursing lingually and then sharply mesially to contact the anterior arm of the hypocone (the metaloph on M2–3 consistently runs mesiolingually toward the metaconule); a relatively well-developed endoloph on M2–3; no cingula on the upper or lower teeth; and a more mesially placed metaconid on DP4.

Description.

Alveoli for a single-rooted tooth placed mesial to DP4 in partial maxillae demonstrate that DP3 was present during life (Fig. 2I). The DP4 (Fig. 2 A, B, and I) is broader than it is long and somewhat quadrate in outline. Overall, the tooth is very similar to that of P. aegyptensis, but bears a mesolophule and, in some individuals, a mure (see Fig. 2B). The metaloph on DP4 is either oriented toward the metaconule or trends toward the posteroloph and then turns mesially to join the metaconule in the middle of the tooth. The posterior arm of the paracone occupies most of the labial wall between the paracone and the metacone; this wall is sometimes interrupted by a distinct mesostyle.

The P4 is relatively small, broader than it is long, and has a short lingual margin, leading to a somewhat triangular outline (Fig. 2 C, J, and L). A small hypocone is situated distal and labial to the protocone and is connected to that cusp by an endoloph. The low anteroloph and relatively high protoloph run labially from the mesial side of the protocone to meet the paracone, enclosing the anterior basin of the tooth, while the metaloph and posteroloph are connected to the hypocone lingually, and to the metacone labially, delimiting the posterior basin of the tooth. The middle basin bears a small conule or lophule that is derived from the lingual part of the metaloph.

The upper molars of Waslamys are also similar to those of P. aegyptensis but have relatively well-developed labial walls and mesolophules, and the former often has a posteriorly oriented metaloph on M1 (Fig. 2 D, E and L) that meets the posteroloph. In some individuals, the metaloph is oriented almost directly lingually, forms a weak connection with the posteroloph, and then turns sharply mesially to meet the metaconule. In some individuals, the mesolophule reaches the labial wall and connects to a tiny mesostyle. As in P. aegyptensis, the lingual sinus on M1 is continuous with the middle basin of the tooth. A small parastyle is present on the most labial part of the anteroloph. The M2 (Fig. 2 F–H, K, and L) has a similar occlusal configuration to that of M1, but tapers posteriorly, has longer and relatively well-developed lophs, taller cusps, a well-developed endoloph, and a metaloph that curves gradually mesiolingually to contact the metaconule. The mure varies from being absent, to incipient, to complete (see Fig. 2H).

The M3 has a heart-shaped outline (see Fig. 2 K and L). The anterior half of the tooth is similar to the corresponding part on M1–2, but the posterior part is much different in having a very reduced metacone and hypocone. The hypocone is placed far labial to the protocone and the posteroloph is relatively short.

The DP4 is only known from 2 isolated teeth (Fig. 2M). The tooth differs from the DP4 of P. aegyptensis primarily in having a more anteriorly positioned metaconid and mesially closed anterior basin. The P4 (Fig. 2 N, O, and W) has a somewhat rectangular outline and 4 major cusps. The hypoconid flares posterolabially. The metaconid is placed transverse to the protoconid, and these cusps are sometimes connected by a complete metalophulid II; in other individuals that crest is short. A low anterolophid connects the metaconid to the protoconid, and a well-developed ectolophid joins the hypoconid to the protoconid. The hypolophid runs labially from the entoconid, but it is interrupted just before reaching the ectolophid. The posterolophid is tall and well developed and courses around the posterior margin of the crown; there is no hypoconulid. The lingual wall is tall and has no accessory cusps.

The lower molars (Fig. 2 P–X) differ very little from those of P. aegyptensis. The metalophulid I is well developed and runs labially from the metaconid to fuse with the anterior side of the protoconid, delimiting the anterior portion of the crown. The anterocingulid is absent. The metalophulid II is short and oriented toward the lingual wall. A well-developed ectolophid runs from the protoconid to attach to the junction of the hypolophid and the anterior arm of the hypoconid. The posterior arm of the metaconid is long, reaching the base of the entoconid and forming most of the lingual wall; in some individuals, there is a notch mesial to the entoconid. On M1–2 (see Fig. 2 P–S, W and X), a well-developed posterolophid bearing a robust hypoconulid courses around the posterior margin of the tooth, connecting the hypoconid and entoconid and closing the posterior basin. A small crest is sometimes present distal to metalophulid II, occasionally connecting to the ectolophid. The posterior basin of the M3 is shorter than that of P. aegyptensis.

The ventral masseteric ridge curves gently from the lateral border of the plane of the incisor in the pattern that is typical of hystricognathous rodents (e.g., see Fig. 2 V–X). The mental foramen opens beneath the anterior root of the P4 at the anterior end of the ventral massetric ridge, as in later Fayum phiomorphs. The dorsal masseteric ridge is also prominent and parallel with the occlusal plane, joining the ventral masseteric ridge to close off the masseteric fossa.

Phylogenetic Analysis.

We added 20 additional stem and crown hystricognathous rodents (including P. aegyptensis and Waslamys), and 7 additional morphological characters to Marivaux et al.'s (14) matrix, and analyzed the interrelationships of stem and crown Hystricognathi using various approaches, including addition of a chronobiogeographic character. Parsimony analysis of morphological features alone in PAUP* 4.0b10 (Fig. S2) recovers a topology that is inconsistent with recent molecular results by nesting Hystricidae within Caviomorpha; this result is also highly unparsimonious biogeographically in implying a South American origin for the clade containing both Hystricidae and the late Eocene African genus Gaudeamus. All of the later Paleogene African rodents are placed as stem hystricognaths, rather than as phiomorphs, as is traditionally thought (4). Parsimony analysis following implementation of a backbone constraint (constraining the South American caviomorphs and the extant phiomorph Thryonomys to be the sister group of Hystricidae) again places all of the Paleogene African rodents as stem hystricognaths. These peculiar results are likely due to the highly autapomorphic molar teeth of extant Thryonomys, which has converged on similarly specialized hystricids and caviomorphs. Both of these analyses most parsimoniously reconstruct an Afro-Arabian origin for crown Hystricognathi.

The topology recovered from our chronobiogeographic analysis (Fig. 3), in which we constrained Oligocene African phiomorphs such as Phiomys, Paraphiomys, and Metaphiomys to be placed closer to the Phiomorpha-Caviomorpha clade than to Hystricidae, is more consistent with previous interpretations in placing Phiomys and Metaphiomys as stem phiomorphs; Thryonomys is nested deep within a phiomorph clade whose earliest members date to ≈34 Ma. Gaudeamus is again placed as a sister taxon of Hystricidae; to our knowledge this is a unique result that has not been previously considered. Protophiomys and Waslamys are placed as consecutive sister taxa of crown Hystricognathi, while all of the Asian baluchimyines fall outside of that clade. Baluchimyines (i.e., Baluchimys, Bugtimys, Hodsahibia, Lindsaya, and Lophibaluchia) are clearly paraphyletic with respect to crown Hystricognathi, and the complex stem lineage of Hystricognathi is expanded to include other enigmatic Paleogene taxa, such as Sacaresia from the Oligocene of Mallorca (27) and Confiniummys and Ottomania from near the Eocene-Oligocene boundary in Turkey (28).

Fig. 3.
Strict consensus of 18 equally parsimonious trees of length 437.3583, derived from parsimony analysis in Mesquite v. 2.6 of a character matrix containing 115 morphological characters, 1 chronobiogeographic character, and 40 characters constraining Hystricidae ...

Molecular Dating.

We used a Bayesian relaxed molecular clock method to date the origin of crown Hystricognathi and the split between Phiomorpha and Caviomorpha. The method was implemented by the mcmctree program of PAML v. 4.2 (29), using Blanga-Kanfi et al.'s (24) recently published DNA sequence dataset, comprised of 6 nuclear genes from 49 taxa. The mean estimates for the nodes of interest (Table S2, Fig. S3, Fig. 4) are about 15% younger that those presented in a recent analysis (19), but are remarkably congruent with the fossil record. The divergence of Caviomorpha and Phiomorpha is estimated to have occurred at 36.1 Ma (95% credibility interval 33.4–39.0 Ma), very close to Opazo's (22) previously published estimate of 36.6 ± 2.5 Ma. Based on the results of our chronobiogeographic analysis, there are no stem phiomorphs present at the ≈37 Ma Locality BQ-2, and the oldest stem phiomorph fossils are found at a ≈34 Ma site [Quarry L-41 (3)]. The oldest caviomorph fossils are at least 31.5 Ma (30), perhaps even older (31), leaving a ≈4 million year-long window for the caviomorph dispersal to South America in either the latest Eocene or earliest Oligocene. The origin of crown Hystricognathi is estimated to be 39.0 Ma (95% credibility interval 36.1–41.9 Ma): that is, ≈2 Ma older than P. aegyptensis and Waslamys. The taxon identified as the oldest stem hystricid in our analysis is ≈34 Ma Gaudeamus, which already has a highly derived dental pattern at the time of its first appearance in the fossil record (4), suggesting a substantial previous phase of evolution in Afro-Arabia. Again, this result would be consistent with an early (≈39 Ma) origin of stem Hystricidae in Africa, but these results contradict a previous analysis that aligned Gaudeamus with extant Thryonomys to the exclusion of highly derived Oligocene and Miocene phiomorphs (32), because our molecular dating results estimate that Thryonomys diverged from Petromus in the early Miocene, around 18 Ma.

Fig. 4.
Molecular clock estimates for divergence dates within Ctenohystrica. Date estimates in Ma appear in white at each node. These estimates are the mean of the posterior distribution. The 95% credibility intervals are represented by thick horizontal bars ...

Discussion

Previously, the oldest known hystricognathous rodent was late Eocene Protophiomys algeriensis from Bir el-Ater in Algeria (33). We consider it likely that P. aegyptensis and Waslamys attiai are at least slightly older than the relatively poorly-dated P. algeriensis, because BQ-2 and nearby contemporaneous localities lack any evidence for the presence of the immigrant artiodactyl family Anthracotheriidae, a group that otherwise makes its first appearance in Afro-Arabia at Bir el-Ater. Furthermore, Jaeger et al. noted that “several species of [undescribed] phiomyids…are recorded in this locality [Bir el-Ater], and they can be related to some of the Oligocene Fayum phiomyids” (ref. 33, p. 575). There are no derived phiomyid taxa at BQ-2, again supporting an earlier age for this level.

Jaeger et al. placed P. algeriensis in the family Phiomyidae, but cautioned that it was “premature to consider these species as closely related phylogenetically. Protophiomys algeriensis can be considered as an upper Eocene primitive morphotype in the evolution of African phiomyids.” (ref. 33, p. 575). The genus was subsequently reevaluated by Flynn et al. as being a “chapattimyid of baluchimyine affinity” (ref. 11, p. 51). Marivaux et al.'s (13) phylogenetic analysis of dental characters found the phiomorph-caviomorph clade to be more closely related to two Oligocene Asian baluchimyine lineages (Bugtimys-Hodsahibia and Lophibaluchia) than to Protophiomys. Their topology implies two independent dispersals of hystricognathous rodents into Afro-Arabia: one from within a paraphyletic “Baluchimyinae” that gave rise to Protophiomys, and another that gave rise to either phiomorphs alone or to a phiomorph-caviomorph clade.

The topology derived from our chronobiogeographic analysis implies that Protophiomys and Waslamys are advanced stem members of Hystricognathi, and that a dispersal from Asia to Afro-Arabia occurred along a deeper portion of the stem lineage of Hystricognathi. The very slight morphological differences separating Asian baluchimyines and the earliest Afro-Arabian taxa, such as Protophiomys and Waslamys, strongly suggests that these taxa record what are, perhaps, the very earliest stages of hystricognathous rodent evolution in Afro-Arabia. This hypothesis is further supported by the lack of morphological diversity observable among the hystricognathous rodents represented at BQ-2. This scenario is clearly not consistent with molecular estimates for the time of origin of crown Hystricognathi that range in age from ≈85 to ≈43 Ma (9, 18, 19, 23, 34).

The temporal and phylogenetic evidence provided by these fossil discoveries, combined with younger molecular estimates for basal divergences within crown Hystricognathi, suggests that the key events determining the distribution of Oligocene-to-Recent hystricognathous rodents occurred between ≈40 and ≈34 million years ago. Afro-Arabia and South America were fully isolated during this interval, so vicariance (31) can clearly be ruled out as a mechanism underlying the divergence between Phiomorpha and Caviomorpha. As appears to have been the case for platyrrhine anthropoids (35), the caviomorph colonization of South America evidently occurred via a chance dispersal from Afro-Arabia across the vast South Atlantic. Future paleontological research in the late middle Eocene of Afro-Arabia and Asia should help to further clarify the later stages of evolution along the stem lineage of Hystricognathi, while recovery of fossils between ≈37 and ≈34 Ma in Afro-Arabia should help to illuminate the nature of the caviomorph-phiomorph split.

Materials and Methods

Phylogenetic analysis was based on a modified version of Marivaux et al.'s (14) morphological character matrix. The chronobiogeographic character takes into account temporal succession of fossil taxa [as in stratocladistics (36)] and also adds a step to tree length for every implied transoceanic dispersal (given reconstructed paleogeography) (37). (See SI Materials and Methods).

Molecular dating was implemented by the mcmctree program of PAML v. 4.2 (29), using Blanga-Kanfi et al.'s (24) DNA sequence dataset, comprised of 6 nuclear genes from 49 taxa (rodents as well as lagomorph and euarchontan outgroups; see SI Materials and Methods). This molecular clock analysis was calibrated with 10 “soft bounds” (38, 39) from the fossil record. Seven of these calibrations were within Rodentia but outside of crown Hystricognathi, which allowed date estimates that were independent of the controversial early fossil record of hystricognathous rodents. Importantly, we considered it likely that, based on the reasonably good early fossil record of stem and crown rodent evolution, crown Rodentia likely did not originate before the K-T boundary. Cretaceous zalambdalestids previously identified as members of Glires (40), and often used as “upper bound” calibrations for the time of origin of Glires in molecular dating analyses (19), are here considered to be stem placentals (41).

Supplementary Material

Supporting Information:

Acknowledgments.

We thank the staff of the Egyptian Mineral Resources Authority and the Egyptian Geological Museum, who provided valuable assistance in Egypt. P. Chatrath managed fieldwork in the Fayum area. H. de Bruijn and L. Marivaux kindly provided casts and photographs and A. Grossman and M. Sánchez-Villagra provided useful comments. D. Boyer, N. Charnley, O. Green, and J. Groenke provided technical assistance. Fieldwork was supported by the United States National Science Foundation and The Leakey Foundation. This work was supported in part by Grant RR003037 from the National Center for Research Resources (to M.E.S.), a component of the National Institutes of Health.

Footnotes

The authors declare no conflict of interest.

This article contains supporting information online at www.pnas.org/cgi/content/full/0908702106/DCSupplemental.

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