Molecular Systematics of Rodents
"Given the considerable amount of parallelism and convergence that is believed to have occurred in virtually all components of the rodent masticatory system, as well as the uncertainties that surround the recognition of homology or homoplasy, we believe that those phylogenetic hypotheses which can be corroborated by data from several different (and preferably unrelated) organ systems are more likely to reflect the true phylogeny of a group, than are those hypotheses corroborated by only a single character complex." (Luckett and Hartenberger 1985)
Currently, Scott Steppan (Florida State University) and I are collaborating on an NSF-funded project to resolve the phylogenetic relationships among members of the family Muridae, which comprise >25% of all mammals. Previously much of my research concerned the molecular systematics of eutherian (placental) mammals and major lineages of rodents.
Significance of rodent systematics
Rodents are extremely important to evolutionary biology, medicine, genomics, ecology, and agriculture. Of the 4,206 species of mammals 1,752 are rodents (42%) and 1,122 are in the family Muridae. In other words, slightly less than half of all mammals are rodents, and almost 27% belong to a single family. Muridae account for >8 million of the nucleotide sequences in GenBank, and over 56,000 articles using rodents were cataloged in PubMed in 2004 alone. The complete sequence of the Mus musculus genome has become a standard for comparative genomics and genome structure. In industrialized countries, rodents consume 1-20% of crops and as much as 50% of crops in less industrialized countries. In Pakistan rodent control produced a 21.4% increase in rice production. In natural environments, rodents account for 50% of the plant material consumed by herbivores and routinely out-consume large herbivores.
Rodents serve as direct or indirect vectors of many human diseases. Plague epidemics have been initiated from fleas carried by Rattus, Meriones, Tatera, and Rhabdomys, and at least 200 other rodents carry plague-bearing fleas. Hantaviruses are an extremely interesting case. At least 13 species in 7 different genera of rodents have directly infected humans or are carriers of various hantavirus strains. Importantly, the phylogeny of hantaviruses parallels the phylogeny of their rodent hosts, implying a long period of coevolution and cospeciation of rodents and viruses. Therefore, a complete understanding of the evolution, ecology and biogeography of hantaviruses requires an accurate understanding of the phylogeny and biogeography of their rodent hosts.
Muridae
"Still it presents the irony that if we devalue or dismiss all characters thought to exhibit homoplasy within the realm of Muroidea, then it is not apparent what evidence remains upon which to ground our phylogenetic hypotheses." (Carleton and Musser 1984)
Superfamily Muroidea (mice, rats, hamsters, voles, gerbils, etc.) contains almost 1/3 of all mammals (>1,300 species), including the most intensively studied nonhuman species in biology. A muroid phylogeny will shed light on many fields of biology. Biomedicine: Muroids are the preeminent biomedical research organisms. Increasingly, researchers are expanding beyond mouse, rat, and hamster to other muroids to interpret findings within an evolutionary context. An accurate phylogeny is essential for correctly interpreting these studies and for identifying taxa for future studies. Biogeography: Muroids inhabit every major landmass except Antarctica and New Zealand, and their phylogeny, biogeography, and speciation dates reveal much about evolution. For example, determining whether sigmodontines entered South America within the last 4 My or much earlier (7-20 Mya) has significant implications for rates of speciation, dispersal, and local adaptation. Similarly, reconstructing the phylogeography of Australasian murines will clarify the faunal evolution of that region. Morphology/ development: Muroids exhibit extraordinary levels of morphological homoplasy, confounding resolution of their relationships but providing “replicate experiments” for statistically powerful comparative studies. Cospeciation: Muroids exhibit patterns of cospeciation with their pathogens (i.e., hantavirus and arenaviruse) or parasites (e.g., lice). Robust phylogenies are necessary to identify patterns of host-parasite coevolution. Molecular evolution/dating: Muroids have a high rate of nucleotide substitution. Combining a robust phylogeny with divergence date estimates that take into account this higher rate of substitution will greatly benefit studies of biogeography, paleontology, and molecular evolution. Comparative genomics/proteomics: Mus and Rattus have complete genome sequences and other muroids will likely be initiated (i.e., Chinese hamster). Correct interpretation of their genome evolution requires a robust phylogeny.
Relationships among the taxa are based primarily on dental morphology, and the problem of inter-relationships is so acute that the subfamilies are currently ranked equally. Murids explosively radiated near the beginning of the Miocene, when the first unambiguous fossils of several subfamilies appear. The rapidity of this radiation is reaffirmed by the lack of well-supported subfamilial associations in molecular studies.
With the recent funding of the National Science Foundation, we are sequencing several gene regions that differ substantially in their rates of substitution and levels of selective constraint (see below).
Based on these gene sequences we have been able to determine the broad outline of the relationships among the subfamilies of murid rodents (below). Now we are engaged in a much deeper investigation of each subfamily, with particular emphasis on the large subfamilies Murinae and Sigmodontinae.
