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Anatomy of the Arvicoline Radiation (Rodentia): Palaeogeographical, Palaeoecological History and Evolutionary Data

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Anatomy of the Arvicoline Radiation (Rodentia): Palaeogeographical, Palaeoecological History and Evolutionary Data Ann. Zool. Fennici 36: 239–267 ISSN 0003-455X Helsinki 17 December 1999 © Finnish Zoological and Botanical Publishing Board 1999 Anatomy of the arvicoline radiation (Rodentia): palaeogeographical, palaeoecological history and evolutionary data Jean Chaline, Patrick Brunet-Lecomte, Sophie Montuire, Laurent Viriot & Frédéric Courant Chaline, J., Brunet-Lecomte, P. & Montuire, S, Biogéosciences-Dijon (UMR CNRS 5561) et Paléobiodiversité et Préhistoire (EPHE), Université de Bourgogne, Centre des Sciences de la Terre, 6 bd. Gabriel, 21000 Dijon, France Courant, F., Biogéosciences-Dijon (UMR CNRS 5561), Université de Bourgogne, Centre des Sciences de la Terre, 6 bd. Gabriel, 21000 Dijon, France Viriot, L., Laboratoire de Géobiologie, Biochronologie et Paléontologie Humaine, Faculté des Sciences Fondamentales et Appliquées, Université de Poitiers, 40 avenue Recteur Pineau, 86022 Poitiers, France Received 30 December 1998, accepted 30 September 1999 Chaline, J., Brunet-Lecomte, P., Montuire, S., Viriot, L. & Courant, F. 1999: Anatomy of the arvicoline radiation (Rodentia): palaeogeographical, palaeoecological history and evolutionary data. — Ann. Zool. Fennici 36: 239–267. Voles and lemmings (Arvicolinae subfamily) diversified throughout the northern hemi- sphere over five million years into 140 lineages. Attempts have been made to identify relationships within the Arvicolinae on the basis of biochemical, chromosomal and mor- phological characteristics as well as on the basis of palaeontological data. Arvicolines are thought to have originated from among the Cricetidae, and the history of voles can be divided into two successive chronological phases occurring in Palaearctic and Nearctic areas. The history of lemmings is not well documented in the fossil record and their Early Pleistocene ancestors are still unknown. The arvicoline dispersal is one of the best known and provides an opportunity to test the anatomy of the radiation and more particularly the punctuated equilibrium model. Study of arvicolines reveals three modes of evolution: stasis, phenotypic plasticity and phyletic gradualism. Clearly the punctuated equilibrium model needs to be supplemented by a further component covering disequilibrium in phenotypic plasticity and phyletic gradualism, suggesting a punctuated equilibrium/dis- equilibrium model. In terms of palaeogeography, study of arvicolines shows that Quater- nary climatic fluctuations led to long-range faunal migrations (3 000 km) and study of these patterns is a significant factor in mapping past environments and climates. Some studies attest to the prevailing influence of ecological and ethological factors on skull morphology in arvicoline rodents sometimes inducing morphological convergences. 240 Chaline et al. • ANN. ZOOL. FENNICI Vol. 36 1. Introduction est cover around the Bering land bridge may have formed an ecological barrier to the migration of Voles and lemmings (Arvicolinae, Rodentia) first these essentially grassland animals. appeared some 5.5 million years ago and have The deliberate historical focus of this presen- diversified over this short geological time-span tation means we must work from palaeontologi- into 140 lineages comprising 37 genera including cal data in their dated stratigraphical context and extinct forms, of which more than a hundred spe- discuss and criticize those data in the light of bio- cies are extant (Miller 1896, Ellerman 1940, Eller- logical data. man & Morrison-Scott 1951, Gromov & Poliakov The term of “arvicoline” has been here cho- 1977, Honacki et al. 1982, Chaline 1974a, 1987): sen following the classification of Wilson and Ree- 143 species in 26 genera (Carleton & Musser 1984, der (1993). 1993). Modern mammalogists place “microtines” as a subfamily (Arvicolinae) within the Muridae (Carleton & Musser 1993). 1.2. The morphological approach to palaeon- tology 1.1. Arvicoline characteristics Voles are useful palaeoecological, palaeoclimat- ical, palaeogeographical and evolutionary indica- Arvicolines include voles and lemmings. Voles tors because they are abundant in fossil and ar- have a long lower incisor that crosses from the chaeological records and in the wild today where lingual to the labial side of the molars between the their prismatic teeth are found in pellets regurgi- bases of the first and second lower molars (M2 and tated by birds of prey (Chaline 1972, Andrews M3) in the rhizodont forms and then rises in the 1990 and J. C. Marquet unpubl.). Unfortunately, lower jaw to germinate at or near the articular con- far too many species have been and still are con- dyle. In lemmings, by contrast, the lower incisor sidered from a typological standpoint with no is very short, entirely lingual relative to the mo- analysis of variability (Kretzoi 1955, 1956, 1969, lars and germinates posteriorly ahead of the M3 Hibbard 1970a, 1972, Rabeder 1981, Fejfar et al. capsule. Since the cricetine incisor runs diagonally 1990). Arvicoline systematics is littered with under the row of molars, the lemming structure names that hamper both the establishment of true seems to be derived and is an apomorphic feature phylogenetic relationships and our understanding (Kowalski 1975, 1977, Courant et al. 1997). of how the group evolved. Fortunately, with bio- Arvicolines are essentially Holarctic rodents. metric studies, biological populations can be com- Their northward distribution is bound by the Arc- pared by using increasingly comprehensive mor- tic Ocean or land ice. Southwards they have rarely phometries (Chaline & Laurin 1986, Brunet- reached the subtropical zone: Guatemala, north- Lecomte & Chaline 1991 and P. Brunet-Lecomte ern Burma, northern India, Israel and Libya. They unpubl.). Recent studies have used image analy- may have occurred in North Africa in Quaternary sis of the occlusal surfaces of teeth (Schmidt- times (Jaeger 1988), if Ellobius is counted among Kittler 1984, 1986, Barnosky 1990, Viriot et al. arvicolines by arguments based on chromosomes 1990). New methods of morphological geometry (Matthey 1964a), but this is much contested and are now employed (Sneath 1967, Rohlf & tends to be refuted by arguments based on lower Bookstein 1990, Bookstein 1991) using Procrustes jaw structure (Repenning 1968). 2.0 software (David & Laurin 1992) to quantify Historycally arvicoline dispersal was control- phenetic differences and convergence between led by geographical barriers and climate (Repen- crania (Courant et al. 1997). ning 1967, 1980, Fejfar & Repenning 1992, Re- New areas of investigation include worldwide penning et al. 1990). For example, the high sea systematics and phylogeny based on dental mor- levels in Pliocene–Pleistocene times that formed phology, enamel structures (von Koenigswald the Bering Strait also flooded low-lying Arctic 1980, von Koenigswald & Martin 1984a, 1984b areas as far away as the Ural Mountains. Before and J. Rodde unpubl.), evolutionary modes and these glaciation-related sea level fluctuations, for- stratigraphical data (Chaline 1984, 1986, Chaline ANN. ZOOL. FENNICI Vol. 36 • Anatomy of the arvicoline radiation (Rodentia) 241 & Farjanel 1990), as well as geographical and cli- biguous forms on the basis of the characters of matic distribution patterns (Chaline 1973, 1981, lower jaw musculature. He claims that arvicolines Chaline & Brochet 1989, Montuire 1996, Montuire are recognised by the following major mandibu- et al. 1997). lar characters: (1) the anterior edge of the ascend- ing ramus originates at, or, anterior to the poste- rior end of M1 and ascends steeply, obscuring all 1.3. Biological approaches or part of M2 in labial aspect; (2) the anterior part of the medial masseter inserts in a narrow groove In addition, arvicolines have been the subject of parallel to the anterior edge of the ascending ra- in-depth biological studies — protein differentia- mus known as the “arvicoline groove”; (3) the tion (Duffy et al. 1978, Graf 1982, Moore & Jana- lower masseteric crest is long, located anteriorly cek 1990), chromosomal formulas (Matthey 1957, and very shelf-like; (4) the internal temporalis Meylan 1970, 1972, Winking & Niethammer fossa forms a broad elongate depression separat- 1970, Chaline & Matthey 1971, 1964b, 1973, ing M2 and M3 from the ascending ramus. Winking 1974, 1976, Niethammer & Krapp 1982, Most of these characters result from shorten- Zagorodnyuk 1990a, 1991), reproduction and ing and deepening of the arvicoline lower jaw ecology (Ognev 1964, Gromov & Poliakov 1977, which strengthens the bite. Chaline & Mein 1979, Carleton & Musser 1984, Repenning’s analysis provides the following Courant et al. 1997) — which have sometimes findings: (1) Microtoscoptes disjunctus (known led to phylogenetic relationships that differ be- from the Middle Pliocene of North America and cause of the independence of rates of evolution at Asia) resembles arvicolines by parallelism and the various levels of integration of the living world. could be considered as an arvicoline “sister group”. It has been shown that genetic and morphological L. D. Martin (1975) described a new and very data are decoupled to varying extents (Chaline & closely related form, Paramicrotoscoptes hibbar- Graf 1988, Brunet-Lecomte & Chaline 1992, Din di, in the Hemphillian (ca. 6.5 Ma) of Nebraska. et al. 1993, Courant et al. 1997). A developmen- A recent revision of material including a study of tal approach has been attempted by using devel- the enamel structure by W. von Koenigswald opmental heterochronies in order to analyse their (Fahlbusch 1987) confirmed that Microtoscoptes impact
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