Muskrat: noble beast, named for its stench. Photo in public domain.

Earlier in the year I made a promise that I’d get through more rodents here at Tet Zoo. Rodents, you see, divide people like no other group of tetrapods. Some hate them, others love them, and while they’ve classically been regarded as bread-and-butter staples of discussions about tetrapod evolution and diversity, others bemoan their sameyness and the fact that most ideas about their history and evolution are based on their cheek teeth. With all of this in mind, I bring you: MORE RODENTS.

Swimming muskrat photographed in Canada; image by D. Gordon E. Robertson, CC BY-SA 3.0.

And today: muskrats. This rodent group is represented in the extant fauna by just a single living species: Ondatra zibethicus, a native of North America introduced by people to South America, Europe and Asia. The combined body and tail length of a muskrat can be 62 cm, and big individuals can weigh as much as 1.8 kg. Thickened enamel with a relatively undifferentiated internal structure is present on the teeth. The scaly tail is somewhat laterally flattened, the hindfeet are partially webbed and have so-called ‘swimming fringes’ of short, stiff, closely spaced hairs along their outer edges. This is an amphibious rodent that eats many different sorts of aquatic and waterside vegetation as well as crustaceans, molluscs and fish. It occurs in numerous different sorts of aquatic habitats, including freshwater ponds, lakes, rivers and marshes as well as brackish marshes and the vegetated edges of estuaries and coasts. It's credited with swimming feats that sound remarkable for a mammal of its size. Nowak (1999) refers to an ability to swim submerged for a distance of 100 m, and to remain submerged for as long as 17 minutes. [Adjacent photo by D. Gordon E. Robertson.]

Here's that (substantially simplified) vole cladogram again, based predominantly on the topology recovered by Galewski et al. (2006). Image by Darren Naish.

Ondatra is – surprising as it might seem, given its size and amphibious lifestyle – a vole, sometimes regarded as distinct enough relative to other voles that it needs its own ‘subfamily’ (Ondatrinae) or ‘tribe’ (Ondatrini) or whatever. Several different phylogenetic hypotheses have been proposed for the vole clade – properly called Arvicolidae (or Arvicolinae if you want to regard voles as part as the same ‘family’ as Cricetidae) – and muskrats have been placed in several possible positions, most recently as close to Arvicola or/and the red-backed voles (Clethrionomys or Myodes) (Conroy & Cook 1999, Galewski et al. 2006, Robovsky et al. 2008).

Muskrat skull (total length c. 60 mm). Photo by Ryan Somma, CC BY-SA 2.0.

The muskrat fossil record is an area of both great controversy and copious data, with different workers having very different ideas at to which taxa the muskrat clade includes. [Adjacent skull photo by Ryan Somma.] Let’s begin by saying that Ondatra (as currently recognised) has a rich and extensive fossil record. Hundreds of fossil Ondatra specimens are known, extending back in time more than 4 million years to the Lower Pliocene. Martin (1993) and some other authors have argued that these all belong to the same single lineage and that they essentially represent different ‘chronomorphs’ of O. zibethicus (formerly, as many as six species were identified, as was the distinct genus Pliopotamys). Not everyone agrees with the taxonomy that Martin employs, of course: the name Pliopotamys is still used by some, and species distinct from O. zibethicus are also still recognised by some authors. Chaline et al. (1999), for example, recognised O. obscurus for an isolated muskrat population from Newfoundland. [Image below by Linda Tanner.]

Nice picture of muskrat eating. Photo by Linda Tanner, CC BY-SA 2.0.

Across the history of this lineage, we see evidence for a marked increase in body size (from c. 100 g to over 1000 g), an increase in tooth complexity (involving the number of triangles and folds and the internal arrangement of enamel layers), an increase in hypsodonty (tooth crown height), and the appearance of cementum (Thaler 1962, Nelson & Semken 1970, Viriot et al. 1993, Martin 1996). These changes did not occur in step with one another, but in mosaic fashion: hypsodonty evolved before the number of triangles proliferated (Chaline et al. 1999), and large size evolved about a million years before cementum was added, for example (Martin 1996). This detailed record of evolutionary change is “one of the best examples of phyletic evolution among terrestrial small mammals” (Martin 2007, p. 493), if not among mammals, and tetrapods, in general.

Phylogenetic hypothesis showing molar evolution in North American muskrats Ondatra (and Pliopotamys), Ogmodontomys and Ophiomys, after Chaline et al. (1999). At top left is an enlarged version of Ondatra zibethicus's molar shape.

Beyond Ondatra, it appears that the Pliocene taxa Ogmodontomys and Cosomys are especially close relatives. Both of these taxa have at times been considered congeneric with the (otherwise European) fossil vole Mimomys; all are similar (remember that we’re mostly talking about fossils that consist only of teeth!) but Mimomys has (so far as I can tell) never been identified as a muskrat. Martin (2007) argued that the undifferentiated molar enamel and simple arrangement of enamel layers in Ogmodontomys differentiates it (and another Pliocene fossil muskrat: Ophiomys) from Mimomys and, rather, links it with Ondatra.

This view of muskrats paints them as an endemic North American radiation that descended from an invasion of Siberian voles that occurred about 5 million years ago (Martin 2007). Successive eastward and southward pulses of these rodents then occurred on several occasions. However, an entirely different view of muskrat evolution has been proposed by authors who imagine the group to include a diversity of additional taxa: the Plio-Pleistocene Eurasian forms Dolomys, Pliomys and Kislangia, the extant Balkan snow vole or Martino’s vole Dinaromys bogdanovi and the also exant Round-tailed muskrat or Florida water-rat Neofiber alleni (Repenning 1982, Repenning et al. 1990).

Balkan snow vole (Dinaromys) in life. Illustration by Darren Naish, coloured by Gareth Monger.

So, what gives? Martin (2007) argued that the Eurasian fossil taxa concerned are very different in enamel structure from Ondatra and don’t even seem close to one another. Ergo, they're not muskrats at all. As for the extant taxa Dinaromys and Neofiber, things are still somewhat up in the air. Dinaromys and Ondatra do share a couple of molar tooth characters, their skulls are alike as goes the region around the eye, they both have a naked stapedial artery (that is, it isn’t enclosed by bone), have an especially long gestation period (compared to other voles), and they’re also united by 11 molecular characters. Accordingly, Robovsky et al. (2008) noted that the position of Dinaromys remains uncertain but did find it, and Neofiber, to group with Ondatra in some of their phylogenetic trees. Modi et al. (1996) also found molecular support for an affinity between Ondatra and Neofiber. You know, I never thought that the idea that the Balkan snow vole and Round-tailed muskrat might really be muskrats was likely to be correct. Now, I’m really not sure.

Arvicolid montage: voles of various sorts, lemmings, muskrats. Image by Darren Naish.

Rodents. It’s where all the big controversies are. Well... it’s sure not (err: turtle origins, snake affinities, squamate interrelations), but it’s certainly one of the places where the data is actually good enough to allow competing views to be properly considered. I meant to publish a lot more on rodents in 2014 but progress has been slow. Sorry about that.

For previous Tet Zoo articles on voles and other rodents, see...

Refs - -

Chaline, J., Brunet-Lecomte, P., Montuire, S., Viriot, L. & Courant, F. 1999. Anatomy of the arvicoline radiation (Rodentia): palaeogeographical, palaeoeocological history and evolutionary data. Annales Zoologici Fennici 36, 239-267.

Conroy, C. J. & Cook, J. A. 1999. MtDNA evidence for repeated pulses of speciation within arvicoline and murid rodents. Journal of Mammalian Evolution 6, 221-245.

Galewski, T., Tilak, M.-K., Sanchez, S., Chevret, P., Paradis, E. & Douzery, E. J. P. 2006. The evolutionary radiation of Arvicolinae rodents (voles and lemmings): relative contribution of nuclear and mitochondrial DNA phylogenies. BMC Evolutionary Biology 2006 6: 80 doi:10.1186/1471-2148-6-80

Martin, R. A. 1993. Evolution of hypsodonty and enamel structure in Plio-Pleistocene rodents. In Martin, R. A. & Barnovsky, A. D. (eds) Morphological Change in Quaternary Mammals of North America. Cambridge University Press, Cambridge, pp. 205-225.

- . 1996. Dental evolution and size change in the North American muskrat: classification and tempo of a presumed phyletic sequence. In Seymour, K. & Stewart, K. (eds) Paleoecology and Paleoenvironment of Late Cenozoic Mammals. University of Toronto Press, pp. 431-457.

- . 2007. Arvicolidae. In Janis, C. M., Gunnell, G. F. & Uhen, M. D. (eds) Evolution of Tertiary Mammals of North America, Vol. 2. Cambridge University Press, Cambridge, pp. 480-497.

Modi, W. S. 1996. Phylogenetic history of LINE-1 among arvicolid rodents. Molecular Biology and Evolution 13, 633641.

Nelson, R. S. & Semken, H. A. 1970. Paleoecological and stratigraphic significance of the muskrat in Pleistocene deposits. Geological Society of America Bulletin 81, 3733-3738.

Nowak, R. M. 1999. Walker’s Mammals of the World, Volume II (Sixth Edition). The John Hopkins University Press, Baltimore and London.

Repenning, C. A. 1982. Classification notes. In Honacki, J. H., Kinman, K. E. & Koeppl, J. W. (eds) Mammal Species of the World: A Taxonomic and Geographic Reference. Allen Press, Lawrence (KS), pp. 484.

- ., Fejfar, O. & Heinrich, W.-D. 1990. Arvicolid rodent biochronology of the Northern Hemisphere. In Fejfar, O. & Heinrich, W.-D. (eds) International Symposium: Evolution, Phylogeny, and Biostratigraphy of Arvicolids (Rodentia, Mammalia). Geological Society, Prague, pp. 385-418.

Robovsky, J., Ricánková, V. & Zrzavy, J. 2008. Phylogeny of Arvicolinae (Mammalia, Cricetidae): utility of morphological and molecular data sets in a recently radiating clade. Zoologica Scripta 37, 571-590.

Thaler, L. 1962. Campangols primitives de l’Ancien et du Nouveau monde. Colloque International du CNRS 104, 387-397.

Viriot, L., Chaline, J., Schaaf, A. & Le Bulangé, E. 1993. Ontogenetic change of Ondatra zibethicus (Arvicolinae, Rodentia) cheek teeth analysed by digital image processing. In Martin, R. A. & Barnovsky, A. D. (eds) Morphological Change in Quaternary Mammals of North America. Cambridge University Press, Cambridge, pp. 373-391.