Kevin C. Rowe

Pliocene colonization and adaptive radiations in Australia and New Guinea (Sahul): Multilocus systematics of the old endemic rodents (Muroidea: Murinae)

The old endemic rodents of Australia and New Guinea (Sahul) represent one or more large adaptive radiations including novel morphological adaptations to aquatic, arboreal, hopping, and arid ecologies. Four tribes recognized among the Sahulian old endemics (Hydromini, Conilurini, Anisomyini, and Uromyini) reflect distinct biogeographic and ecomorphological hypotheses about diversification within the Old Endemics. We present the first character-based phylogeny of the Sahulian Old Endemic rodents with broad sampling, nested within a broader phylogeny of the Murinae. We estimated phylogenies from >2,500 nucleotides of mtDNA sequence and >9,500 nucleotides from six autosomal nuclear loci, for individual genes and for the full concatenated data using parsimony, likelihood, and Bayesian methods. Our results strongly supported monophyly of the group and its sister relationship to the Philippine old endemics of the Chrotomys division. Most striking was the rapid diversification after the Late Miocene or Early Pliocene colonization of New Guinea from the west, consistent with a single colonization of the Sahulian continent. That was followed 2-3 My later by a second adaptive radiation resulting from one or more colonizations of Australia. Monophyly was not supported for the Anisomyini or the Conilurini but was for the Uromyini nested within the Conilurini and for the Hydromyini. Conflict among gene phylogenies was weak, and support for the consensus topology increased with more (even conflicting) data.

Multiple geographic origins of commensalism and complex dispersal history of black rats

The Black Rat (Rattus rattus) spread out of Asia to become one of the worlds worst agricultural and urban pests, and a reservoir or vector of numerous zoonotic diseases, including the devastating plague. Despite the global scale and inestimable cost of their impacts on both human livelihoods and natural ecosystems, little is known of the global genetic diversity of Black Rats, the timing and directions of their historical dispersals, and the risks associated with contemporary movements. We surveyed mitochondrial DNA of Black Rats collected across their global range as a first step towards obtaining an historical genetic perspective on this socioeconomically important group of rodents. We found a strong phylogeographic pattern with well-differentiated lineages of Black Rats native to South Asia, the Himalayan region, southern Indochina, and northern Indochina to East Asia, and a diversification that probably commenced in the early Middle Pleistocene. We also identified two other currently recognised species of Rattus as potential derivatives of a paraphyletic R. rattus. Three of the four phylogenetic lineage units within R. rattus show clear genetic signatures of major population expansion in prehistoric times, and the distribution of particular haplogroups mirrors archaeologically and historically documented patterns of human dispersal and trade. Commensalism clearly arose multiple times in R. rattus and in widely separated geographic regions, and this may account for apparent regionalism in their associated pathogens. Our findings represent an important step towards deeper understanding the complex and influential relationship that has developed between Black Rats and humans, and invite a thorough re-examination of host-pathogen associations among Black Rats.

Ecological Opportunity and Incumbency in the Diversification of Repeated Continental Colonizations by Muroid Rodents

Why some clades are more species-rich than others is a central question in macroevolution. Most hypotheses explaining exceptionally diverse clades involve the emergence of an ecological opportunity caused by a major biogeographic transition or evolution of a key innovation. The radiation of muroid rodents is an ideal model for testing theories of diversification rates in relation to biogeography and ecological opportunity because the group is exceptionally species-rich (comprising nearly one-third of all mammal species), it is ecologically diverse, and it has colonized every major landmass except New Zealand and Antarctica, thus providing multiple replicate radiations. We present an extension of the conventional ecological opportunity model to include a geographic incumbency effect, develop the largest muroid phylogeny to date, and use this phylogeny to test the new model. The nearly 300-species phylogeny based on four nuclear genes is robustly resolved throughout. Consistent with the fossil record, we identified Eurasia as the most likely origin of the group and reconstructed five to seven colonizations of Africa, five of North America, four of Southeast Asia, two of South America, two of Sahul, one of Madagascar, and eight to ten recolonizations of Eurasia. We accounted for incomplete taxon sampling by using multiple statistical methods and identified three corroborated regions of the tree with significant shifts in diversification rates. In several cases, higher rates were associated with the first colonization of a continental area, but most colonizations were not followed by bursts of speciation. We found strong evidence for diversification consistent with the ecological opportunity model (initial burst followed by density-dependent slowdown) in the first colonization of South America and partial support for this model in the first colonization of Sahul. Primary colonizers appear to inhibit the ultimate diversity of secondary colonizers, a pattern of incumbency that is consistent with ecological opportunity, but they did not inhibit initial diversification rates of secondary colonizers. These results indicate that ecological opportunity may be a general but weak process in muroids and one that requires specific circumstances to lead to an adaptive radiation. The total land area, length of time between colonizations, and rank of colonizations did not influence the diversification rates of primary colonizers. Models currently employed to test ecological opportunity do a poor job of explaining muroid diversity. In addition, the various rate-shift metrics identified different clades, suggesting that caution should be used when only one is applied, and we discuss which methods are most appropriate to address different questions of diversification.

Recent and Rapid Speciation with Limited Morphological Disparity in the Genus Rattus

Recent and rapid radiations provide rich material to examine the factors that drive speciation. Most recent and rapid radiations that have been well-characterized involve species that exhibit overt ecomorphological differences associated with clear partitioning of ecological niches in sympatry. The most diverse genus of rodents, Rattus (66 species), evolved fairly recently, but without overt ecomorphological divergence among species. We used multilocus molecular phylogenetic data and five fossil calibrations to estimate the tempo of diversification in Rattus, and their radiation on Australia and New Guinea (Sahul, 24 species). Based on our analyses, the genus Rattus originated at a date centered on the Pliocene-Pleistocene boundary (1.84-3.17 Ma) with a subsequent colonization of Sahul in the middle Pleistocene (0.85-1.28 Ma). Given these dates, the per lineage diversification rates in Rattus and Sahulian Rattus are among the highest reported for vertebrates (1.1-1.9 and 1.6-3.0 species per lineage per million years, respectively). Despite their rapid diversification, Rattus display little ecomorphological divergence among species and do not fit clearly into current models of adaptive radiations. Lineage through time plots and ancestral state reconstruction of ecological characters suggest that diversification of Sahulian Rattus was most rapid early on as they expanded into novel ecological conditions. However, rapid lineage accumulation occurred even when morphological disparity within lineages was low suggesting that future studies consider other phenotypes in the diversification of Rattus.

Museum genomics: low-cost and high-accuracy genetic data from historical specimens

Natural history collections are unparalleled repositories of geographical and temporal variation in faunal conditions. Molecular studies offer an opportunity to uncover much of this variation; however, genetic studies of historical museum specimens typically rely on extracting highly degraded and chemically modified DNA samples from skins, skulls or other dried samples. Despite this limitation, obtaining short fragments of DNA sequences using traditional PCR amplification of DNA has been the primary method for genetic study of historical specimens. Few laboratories have succeeded in obtaining genome‐scale sequences from historical specimens and then only with considerable effort and cost. Here, we describe a low‐cost approach using high‐throughput next‐generation sequencing to obtain reliable genome‐scale sequence data from a traditionally preserved mammal skin and skull using a simple extraction protocol. We show that single‐nucleotide polymorphisms (SNPs) from the genome sequences obtained independently from the skin and from the skull are highly repeatable compared to a reference genome.

Segregating Variation in the Transcriptome: Cis Regulation and Additivity of Effects

Properties of genes underlying variation in complex traits are largely unknown, especially for variation that segregates within populations. Here, we evaluate allelic effects, cis and trans regulation, and dominance patterns of transcripts that are genetically variable in a natural population of Drosophila melanogaster. Our results indicate that genetic variation due to the third chromosome causes mainly additive and nearly additive effects on gene expression, that cis and trans effects on gene expression are numerically about equal, and that cis effects account for more genetic variation than do trans effects. We also evaluated patterns of variation in different functional categories and determined that genes involved in metabolic processes are overrepresented among variable transcripts, but those involved in development, transcription regulation, and signal transduction are underrepresented. However, transcripts for proteins known to be involved in protein–protein interactions are proportionally represented among variable transcripts.

A genomewide assessment of inbreeding depression: gene number, function, and mode of action.

Although the genetic basis of inbreeding depression is still being debated, most fitness effects are thought to be the result of increased homozygosity for recessive or partially recessive deleterious alleles rather than the loss of overdominant genes. It is unknown how many loci are associated with inbreeding depression, the genes or gene pathways involved, or their mode of action. To uncover genes associated with variation in fitness following inbreeding, we generated a set of inbred lines of Drosophila melanogaster for which only the third chromosome varied among lines and measured male competitive reproductive success among these lines to estimate inbreeding depression. Male competitive reproductive success for different lines validated our prediction that equally inbred lines show variation in inbreeding depression. To begin to assess the molecular basis of inbreeding depression for male competitive reproductive success, we detected variation in whole-genome gene expression across these inbred lines with commercially available high-density oligonucleotide microarrays. A total of 567 genes were differentially expressed among these inbred lines, indicating that inbreeding directly or indirectly affects a large number of genes: genes that are disproportionately involved in metabolism, stress and defense responses. Subsequently, we generated a set of outbred lines by crossing the highest inbreeding depression lines to each other and contrasted gene expression between parental inbred lines and F(1) hybrids with transcript abundance as a quantitative phenotype to determine the mode of action of the genes associated with inbreeding depression. Although our results indicated that approximately 75% of all genes involved in inbreeding depression were additive, partially additive, or dominant, about 25% of all genes expressed patterns of overdominance. These results should be viewed with caution given that they may be confounded by issues of statistical inference or associative overdominance.

Comparative phylogeography of eastern chipmunks and white-footed mice in relation to the individualistic nature of species

Palaeoecological studies have demonstrated that ecological communities as a whole did not remain stable throughout the climatic fluctuations of the Quaternary. The result is that long‐term associations of species cannot be inferred by contemporary associations in ecological communities. Therefore, the evolutionary significance of any contemporary ecological interactions among species and of the biotic community within which species have evolved also cannot be assumed from contemporary conditions. Comparative phylogeographic data provide a method to identify species within ecological communities that have shared biogeographic histories. We present an example of a long‐term association between populations of two mammalian species, eastern chipmunks (Tamias striatus) and white‐footed mice (Peromyscus leucopus), which are commonly associated with deciduous forest habitats. The distribution of mitochondrial DNA variation in T. striatus and P. leucopus from previously glaciated regions of the eastern United States support the hypothesis that, in at least part of their range, genetic lineages of the two species have expanded from similar population sources since the Last Glacial Maximum. In addition, the spatial concordance of genetic lineages of T. striatus and P. leucopus with the oak‐savannah forest formations of Wisconsin and Illinois, suggest that populations associated with this community colonized the area in association with a set of arboreal species that comprise their deciduous forest habitat.

Cryptic genetic diversity in Rattus of the San Francisco Bay region, California

Invasive species can have complex invasion histories, harbor cryptic levels of diversity, and pose taxonomic problems for pest management authorities. Roof rats, Rattus rattus sensu lato, are common invasive pests of the San Francisco Bay Area in California, USA. They are a significant health risk and pest management efforts impose a large financial investment from public institutions and private individuals. Recent molecular genetic and taxonomic studies of black rats in their native range in Asia have shown that the species is a complex of two karyotypic forms and four mitochondrial genetic lineages that may represent four distinct species. We used mtDNA sequences and nuclear microsatellite variation to identify which mitochondrial lineages of the R. rattus group are present in the San Francisco Bay Area and to test for gene flow among them. We recovered specimens with mtDNA sequences representing two of the major mtDNA lineages of the R. rattus group. Microsatellite variation, however, was not structured in concordance with mtDNA lineages, suggesting a more complex history involving hybridization and introgression between these lineages. Although Aplin et al. (2011) and Lack et al. (2012) reported R. rattus Lineage II in North America, this is the first detailed examination of possible gene flow amongst lineages in this region.

Iridescent colour production in hairs of blind golden moles (Chrysochloridae)

Relative to other metazoans, the mammalian integument is thought to be limited in colour. In particular, while iridescence is widespread among birds and arthropods, it has only rarely been reported in mammals. Here, we examine the colour, morphology and optical mechanisms in hairs from four species of golden mole (Mammalia: Chrysochloridae) that are characterized by sheens ranging from purple to green. Microspectrophotometry reveals that this colour is weak and variable. Iridescent hairs are flattened and have highly reduced cuticular scales, providing a broad and smooth surface for light reflection. These scales form multiple layers of light and dark materials of consistent thickness, strikingly similar to those in the elytra of iridescent beetles. Optical modelling suggests that the multi-layers produce colour through thin-film interference, and that the sensitivity of this mechanism to slight changes in layer thickness and number explains colour variability. While coloured integumentary structures are typically thought to evolve as sexual ornaments, the blindness of golden moles suggests that the colour may be an epiphenomenon resulting from evolution via other selective factors, including the ability to move and keep clean in dirt and sand.