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

Abstract

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.

A Systematic Review of SulawesiBunomys(Muridae, Murinae) with the Description of Two New Species

“…Both of those clades connect phylogenetically to an assemblage containing Philippine Bullimus and Sundaic Sundamys (Fabre et al, 2013). The alliance of Bunomys with Paruromys, Sundamys, and Bullimus is also substantiated by Fabre et al (2012) and Schenk et al [2013] using DNA sequences, and the association of Bunomys with Taeromys, Paruromys, and Sundamys was earlier postulated by Misonne (1969: 140) based on molar cusp patterns. Many of the generic and specific traits described here are those associated with a skin and associated skull-one of the standard museum preparations.…”

The effects of island ontogeny on species diversity and phylogeny

“…We therefore believe that the DD version of our model is the most biologically realistic implementation. An important mechanism through which a negative feedback of diversity on community assembly rates may operate is through geographical incumbency, where the diversification of primary colonists inhibits the ultimate diversity of closely related secondary colonizers [42,43]. Indeed, niche pre-emption effects on rates of immigration and speciation have been reported from a variety of insular environments and taxa [44,45].…”

Using phylogenetic clade composition to understand biogeographical variation in functional traits

“…The largest burst of radiation for this group occurred in South America, where 86 genera and ~400 extant species exist (Patton et al 2015). Sigmodontines rapidly diversified (~10 Ma, Schenk et al 2013) to occupy virtually all Neotropical habitats, with high local richness and turnover throughout South America (Maestri and Patterson 2016). Moreover, the principal monophyletic clades within Sigmodontinae show complementary distributions in South America (Maestri and Patterson 2016), making sigmodontines an ideal group in which to investigate large scale patterns of trait variation at the level of assemblage.…”