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Laonastes and the "Lazarus Effect" in Recent Mammals

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Science  10 Mar 2006:
Vol. 311, Issue 5766, pp. 1456-1458
DOI: 10.1126/science.1124187

Abstract

The living Laotian rodent Laonastes aenigmamus, first described in early 2005, has been interpreted as the sole member of the new family Laonastidae on the basis of its distinctive morphology and apparent phylogenetic isolation from other living rodents. Here we show that Laonastes is actually a surviving member of the otherwise extinct rodent family Diatomyidae, known from early Oligocene to late Miocene sites in Pakistan, India, Thailand, China, and Japan. Laonastes is a particularly striking example of the “Lazarus effect” in Recent mammals, whereby a taxon that was formerly thought to be extinct is rediscovered in the extant biota, in this case after a temporal gap of roughly 11 million years.

In recent years, tropical southeast Asia has been recognized as an important “hot spot” for modern biological diversity (1). The latest addition to the mammalian biota of this hot spot is the rodent Laonastes aenigmamus, recently described by scientists working on a biodiversity survey in Laos (2). Initial investigations of its morphological and molecular affinities established that Laonastes is phylogenetically divergent from other living rodents, which led to its classification in the new family Laonastidae. Current knowledge of Laonastes, known locally as the khanyou, is based on whole specimens that were purchased in local markets and individual bones collected from owl pellets and cave deposits. Although living individuals have yet to be observed by biologists, Laonastes seems to be nocturnal in its activity pattern and is thought to inhabit karstic terrain. It has a vaguely squirrel-like appearance, with an elongated head, pelage ranging from black to grizzled, and a long hairy tail. Its jaws and dentition are highly distinctive, having an enlarged hystricomorphous infraorbital foramen, lacking development of the coronoid process on the mandible, and having distinctly bilophodont cheek teeth. The postcranial skeleton, on the other hand, is generalized, suggesting a scampering mode of locomotion.

Although initial phylogenetic results indicated that Laonastes pertains to an ancient phylogenetically isolated lineage of rodents, morphological comparisons with fossil rodents have not been undertaken previously. Our familiarity with the fossil record of Asian rodents led us to make extensive comparisons between Laonastes and the otherwise extinct Diatomyidae, known from early Oligocene to late Miocene strata in Pakistan, India, Thailand, China, and Japan (310). Three fossil genera—Fallomus, Diatomys, and Willmus—are currently recognized in the Diatomyidae. Fallomus is known from isolated teeth and fragments of jaws from the Oligocene and early Miocene of Pakistan, India, and Thailand (4, 7, 8), whereas the poorly documented Willmus is known from two isolated teeth from the late Miocene of Pakistan (10). Diatomys, on the other hand, is better known and more widely distributed, having Miocene records in Shandong and Jiangsu provinces in eastern China, Kyushu Island in Japan, northern Pakistan, and the Lamphun district of Thailand (3, 5).

Diatomys shantungensis was originally described from the late early Miocene Shanwang Series of Shandong Province, China, based on two relatively complete (but laterally compressed) partial skeletons (3). The well-preserved dentitions of these specimens show that the cheek teeth in each jaw quadrant include one premolar and three molars displaying a simple transversely bilophodont occlusal pattern. Details of cranial and mandibular anatomy were difficult to interpret because of the lateral compression of the fossils. However, Diatomys was originally thought to have an unenlarged infraorbital foramen (the sciuromorphous condition) and a sciurognathous lower jaw. Its postcranial skeleton lacks any obvious morphological adaptations for either leaping or burrowing.

In June 2005, a new and less compressed specimen of D. shantungensis was discovered from the type locality in Shandong Province. The new specimen, IVPP V12692, complete with whiskers and traces of pelage (Fig. 1, A to C), clarifies aspects of the cranial and mandibular anatomy of Diatomys that were either missing or obscured by postmortem deformation in previously described specimens of this species. IVPP V12692 shows that the infraorbital foramen of Diatomys is very large; hence, Diatomys resembles Laonastes (Fig. 1D) in having the hystricomorphous condition. IVPP V12692 also shows that the mandible lacks a coronoid process and has a relatively low condyle; the masseteric fossa extends forward to a level below p4; an anteroposterior ridge, the linea obliqua, separates dorsal and ventral portions of the masseteric fossa; the angular process is in the same vertical plane as the incisor (the sciurognathous condition); the angular process extends posteriorly as far as the condylar process; the ventral side of the angular process is very slightly inflected; and the incisor root is short, extending posteriorly to a level below m2. Thus, the new specimen demonstrates that the mandibles of Diatomys and Laonastes are virtually identical in sharing the following derived characters: absence of a coronoid process, masseteric fossa extending forward to below p4, masseteric fossa subdivided into dorsal and ventral sections, condyle low but higher than tooth row, and shortened incisor.

Fig. 1.

Morphological characters of Diatomys and Laonastes. (A and B) Right side of skull and (C) articulated skeleton of D. shantungensis (IVPP V12692) from the early Miocene, Shandong Province, China. Abbreviations on the skeleton are as follows: cl, clavicle; fe, femur; h, right humerus; lh, left humerus; lv, lumbar vertebrae; ma, manus; pe, pelvis; ri, ribs; ru, right ulna; s, scapula; sc, sternal cartilage; sk, skull; st, sternum; tv, thoracic vertebrae; and vi, vibrissae. (D to G) L. aenigmamus. (D) Right lateral view of skull and mandible of specimen BMNH 1999.71. (E) Scanning electron photomicrographs of lower incisor enamel of BMNH 1998.407, showing the multiserial condition. (Top) Longitudinal section including the total enamel thickness (∼310 μm) with moderately thin radial enamel of the portio externa (PE) and thick (80%) portio interna (PI) with HSBs; the straight HSBs are inclined at about 50° to the enamel-dentine junction at right; scale bar, 100 μm. (Bottom) Details of the PI, showing decussating HSBs with three to four prisms per band and the well-marked transition zone between adjacent decussating HSBs; a thin interprismatic matrix (IPM) never surrounds the prisms but appears as inter-row sheets running at a high angle (≥80°, nearly rectangular) to the prism direction and never anastomoses between the prisms; scale bars, 10 μm. The pattern of the IPM typifies a derived multiserial subtype III. (F) Occlusal view of left mandible of BMNH 1998.408, showing three roots of p4 and four roots of lower molars. (G) Ventral view of sciurognathous left mandible of BMNH 1999.71, with a dashed line showing the position of the lower incisor.

Laonastes was originally described as having a hystricognathous mandible (2). A reexamination of pertinent specimens shows that Laonastes actually has a sciurognathous mandible like that of Diatomys (Fig. 1, D and G). Another characteristic of hystricognathous rodents was also attributed to Laonastes in the original description: a groove for passage of the pars reflexa of the masseter superficialis muscle to its insertion on the medial surface of the angle. Reexamination of specimens of Laonastes revealed no space for this groove in its sciurognathous jaw.

Only heavily worn teeth of Laonastes are currently available for investigation. Nevertheless, the cheek teeth of Laonastes are clearly bilophodont, a condition that also characterizes Diatomys. The acquisition of bilophodonty occurred within Diatomyidae, because Oligocene species of Fallomus have cuspate cheek teeth showing derivation of the bilophodont pattern from a more generalized rodent dental morphology (4, 7, 8). The cheek teeth of Laonastes have elongated crowns that have been described as hypsodont. A highly unusual aspect of the dentition that Laonastes shares with fossil diatomyids is the presence of supernumerary roots on the cheek teeth. In Laonastes, the upper cheek teeth each have three roots, but their size and disposition are unusual for rodents. The upper cheek teeth of Laonastes bear an enlarged U-shaped anterior root and two posterior roots, whereas the lower dentition shows that three roots are present on p4 and four occur on m1-3 (Fig. 1F). In Diatomys, the upper molars each have four roots, whereas the number of roots supporting the lower dentition is identical to that of Laonastes (3, 5). Molars of Fallomus exhibit some variation in the number of roots, but they typically have four (7). This proliferation of roots is derived among rodents, in which the primitive condition has three roots on P4-M3 (including two buccal roots and one larger lingual root) and two roots (one anterior and one posterior) on p4-m3. Given that four roots support the upper cheek teeth of Diatomys and Fallomus, the enlarged U-shaped anterior root on the upper cheek teeth of Laonastes probably resulted from the coalescence of the two anterior roots that occur in fossil diatomyids.

The microstructure of incisor enamel in Fallomus and Diatomys is multiserial, a condition that also characterizes ctenodactylid, pedetid, and hystricognath rodents (5, 8). Although the original description of Laonastes failed to consider this character, our analysis of incisor enamel microstructure in Laonastes revealed the presence of multiserial enamel in this taxon as well (Fig. 1E). Incisor enamel microstructure in Laonastes is very similar to that of Diatomys in having the same number of prisms per Hunter-Schreger band (HSB) and in showing the same degree of complexity of the interprismatic matrix (inter-row sheets running at a high angle to the prism direction and a well-marked transition zone between adjacent decussating HSBs). It differs, however, in showing the HSBs to be much more inclined (>50°) to the enamel-dentine junction than is the case in Diatomys (25° to 30°), a difference that is not unexpected given the large temporal gap between these genera.

Other skeletal similarities between extinct diatomyids and Laonastes can be added to those of the mandible and dentition. Laonastes has a separate neurovascular canal within the orbit. This feature is not interpretable in available specimens of D. shantungensis, but the Oligocene Fallomus also has a separate neurovascular canal, demonstrating early establishment of this character in diatomyids (7). Diatomys and Laonastes are the same size, with head and body length spanning roughly 250 mm, followed by a long tail composed of 20 to 25 caudal vertebrae. Diatomys and Laonastes also share the following postcranial characters: the humerus has a reduced deltoid ridge and a wide distal end and lacks an entepicondylar foramen; the lesser trochanter of the femur is mostly posterior in position; and the astragalus has a sharp medial keel, wide body, and short neck (2, 3, 5). Our phylogenetic analysis of morphological data from various living and extinct rodents identifies Laonastes as a member of Diatomyidae, being more closely related to Diatomys than the latter is to Fallomus (Fig. 2 and supporting online material). We therefore synonymize Laonastidae with Diatomyidae (11).

Fig. 2.

Simplified phylogeny (see supporting online material) showing temporal and geographic distributions of diatomyids. (Top) Suggested relationships of diatomyids within Rodentia, showing occlusal views of right p4-m3 (anterior end to right) of Fallomus, Diatomys, and Laonastes. (Bottom) Geographic distribution of Fallomus (black circles), Diatomys (asterisks), Willmus (white circle), and Laonastes (red circle).

The discovery of the living diatomyid rodent Laonastes offers a rare opportunity to compare phylogenetic results that were derived independently from neontological and paleontological data sets. To date, phylogenetic analyses of genetic data from Laonastes have yielded conflicting results, but a combined analysis of mitochondrial data from 12S ribosomal RNA and cytochrome b places Laonastes as a basal member of Hystricognathi (2). Further molecular analyses should be undertaken, especially in light of the antiquity of the phylogenetic branching events postulated here for this rodent. A recent analysis of morphological data recognized diatomyids as one of several extinct outgroups of living Hystricognathi (12). Of these outgroups, it is striking that the diatomyids continued to evolve in Asia, while the ctenodactylids became extinct in southern Asia but evolved subsequently in Africa. Given the diversity of extinct Asian rodents that apparently lie near the base of the modern radiation of Hystricognathi, Laonastes strengthens paleobiogeographic hypotheses proposing that this group of mainly African and South American extant rodents originated in Asia (6).

The “Lazarus effect” refers to the reappearance of taxa after a lengthy hiatus in the fossil record (13, 14). The discovery of living examples of taxa that were previously thought to be extinct is a very special case of the Lazarus effect, one that has only rarely been documented among mammals and other vertebrates. With the exception of microbiotheriid marsupials (15), all fossil mammal taxa that were subsequently found to be alive have been Pleistocene in age and congeneric with their modern counterparts (16). Uniquely among placental mammals, Laonastes pertains to a clade (Diatomyidae) that was formerly believed to have been extinct for more than 11 million years. Diatomyids join tree shrews, flying lemurs, and tarsiers as examples of ancient and formerly wider-ranging mammalian taxa that are currently living with relictual distributions in southeast Asia.

From a paleontological and phylogenetic perspective, efforts to conserve Laonastes, the sole survivor of a morphologically distinctive family of rodents with deep evolutionary roots in Asia, should be given the highest priority. If it can be preserved, the Paleogene zoo that survives today in southeast Asia can offer invaluable insights regarding past and present biodiversity.

Supporting Online Material

www.sciencemag.org/cgi/content/full/311/5766/1456/DC1

Materials and Methods

SOM Text

Fig. S1

References

References and Notes

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