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The Ecology of a Continental Evolutionary Radiation: Is the Radiation of Sigmodontine Rodents Adaptive?

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The Ecology of a Continental Evolutionary Radiation: Is the Radiation of Sigmodontine Rodents Adaptive? ORIGINAL ARTICLE doi:10.1111/evo.13155 The ecology of a continental evolutionary radiation: Is the radiation of sigmodontine rodents adaptive? Renan Maestri,1,2,3 Leandro Rabello Monteiro,4 Rodrigo Fornel,5 Nathan S. Upham,2,6 Bruce D. Patterson,2 and Thales Renato Ochotorena de Freitas1,7 1Programa de Pos-Graduac´ ¸ao˜ em Ecologia, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS 91501, Brazil 2Integrative Research Center, Field Museum of Natural History, Chicago, Illinois 60605 3E-mail: [email protected] 4Laboratorio´ de Cienciasˆ Ambientais, CBB, Universidade Estadual do Norte Fluminense, Campos dos Goytacazes, RJ 28013, Brazil 5Programa de Pos-Graduac´ ¸ao˜ em Ecologia, Universidade Regional Integrada do Alto Uruguai e das Missoes,˜ Campus Erechim, RS 99709, Brazil 6Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut 06511 7Departamento de Genetica,´ Universidade Federal do Rio Grande do Sul, Porto Alegre, RS 91501, Brazil Received April 26, 2016 Accepted December 10, 2016 Evolutionary radiations on continents are less well-understood and appreciated than those occurring on islands. The extent of ecological influence on species divergence can be evaluated to determine whether a radiation was ultimately the outcome of divergent natural selection or else arose mainly by nonecological divergence. Here, we used phylogenetic comparative methods to test distinct hypotheses corresponding to adaptive and nonadaptive evolutionary scenarios for the morphological evolution of sigmodontine rodents. Results showed that ecological variables (diet and life-mode) explain little of the shape and size variation of sigmodontine skulls and mandibles. A Brownian model with varying rates for insectivory versus all other diets was the most likely evolutionary model. The insectivorous sigmodontines have a faster rate of morphological evolution than mice feeding on other diets, possibly due to stronger selection for features that aid insectivory. We also demonstrate that rapid early-lineage diver- sification is not accompanied by high morphological divergence among subclades, contrasting with island results. The geographic size of continents permits spatial segregation to a greater extent than on islands, allowing for allopatric distributions and escape from interspecific competition. We suggest that continental radiations of rodents are likely to produce a pattern of high species diversification coupled with a low degree of phenotypic specialization. KEY WORDS: Disparity through time, evolutionary models, evolutionary rates, macroevolution, macroevolutionary adaptive landscape, Neotropics, nonadaptive radiation, tempo and mode of evolution. Understanding the processes of speciation and the origin of adap- arise following ecological specialization with concurrent pheno- tive forms has long attracted the attention of biologists (e.g., Dar- typic diversification (Simpson 1944) or else may arise mainly by win 1859). Events in which many species appear over short time allopatric effects and historical contingencies without disruptive periods are termed evolutionary radiations (Schluter 2000). Such selection (Gould and Lewontin 1979; Rundell and Price 2009). A radiations can be either adaptive or nonadaptive. Species may radiation is considered adaptive if it involves the differentiation of a single ancestor into an array of species that occupy a variety This article corresponds to Bryan S. M. (2017), Digest: Splendid (continen- of niches and differ in the phenotypic traits used to exploit these tal) radiations. Evolution. DOI:10.1111/evo.13183. C 2016 The Author(s). Evolution C 2016 The Society for the Study of Evolution. 610 Evolution 71-3: 610–632 EVOLUTIONARY RADIATION ON A CONTINENTAL SCALE resources (Futuyma 1998; Losos 2010; Losos and Mahler 2010). morphological evolution as niches become filled (Schluter 2000; Rapid speciation resulting in many species that lack accompa- Tran 2014). Ancestors would have abundant resources and many nying phenotypic diversification is best termed a nonadaptive vacant niches to fill, and speciation would produce descendants radiation (Gittenberger 1991; Rundell and Price 2009). that occupy distinct niches in various adaptive zones; later, when Schluter (2000) established four criteria to define a radiation the niches are almost all filled and the rate of novel niche occupa- as adaptive: common ancestry, phenotype–environment correla- tion declines, there should be a corresponding decline in rates of tion, trait functionality, and rapid speciation. Assessing these cri- phenotypic diversification (Simpson 1944; Schluter 2000; Losos teria and understanding the drivers of phenotypic differentiation 2010). Recent evidence suggests that this phenomenon may be in major radiations have been the focus of several macroevo- rarer than previously thought (Harmon et al. 2010; Venditti et al. lutionary investigations (e.g., Grant and Grant 2008; Losos and 2011). Early burst is also not a necessary feature of adaptive radi- Ricklefs 2009; Mahler et al. 2013). Most of these studies have ations (Givnish 2015) and its generality needs to be further tested been conducted on islands, because of the theoretical and practical (Stroud and Losos 2016). Harmon et al. (2003) proposed that if advantages of simple insular systems (Whittaker and Fernandez-´ taxa rapidly diversify early in their history, they should quickly Palacios 2007) compared to the complexities of this kind of study fill ecological niches, so that little subsequent ecological diversifi- with richer biotas at continental scales (Schluter 2000; Clara- cation is expected inside the extant subclades. Under this hypoth- munt 2010; Harmon et al. 2010). Continental radiations may also esis, most morphological variation would exist among subclades, present different macroevolutionary patterns from those studied in characterizing a mostly adaptive radiation (Tran 2014). On the islands, offering new and more extensive empirical information other hand, for taxa that diversify gradually throughout their his- for the study of evolutionary radiations. At continental scales, tory, species may diversify independently of each other, leading studies on Neotropical lizards (Pincheira-Donoso et al. 2015), to greater disparity within rather than among subclades, a pat- passerines (Claramunt 2010), and bats (Monteiro and Nogueira tern mostly characteristic of nonadaptive radiations. We test that 2011) showed that ecological opportunity (the exploitation of hypothesis by comparing patterns of lineages through time and resources underused by other species) plays a strong role in deter- morphological DTT to a major radiation of rodents that colonized mining morphological evolution through the existence of distinct and diversified over the entire Neotropical region and adjacent adaptive peaks. These studies are among the first to apply the parts of North America. concept of Simpson’s macroevolutionary landscape to the phylo- Rodents are the most successful group in the 200-million- genies of continental radiations. year history of mammals. They comprise more than 40% of all Other studies on continental radiations have shown a more living species and occupy most terrestrial environments (Lacher varied relationship between adaptive divergence and ecological et al. 2016). The rodent skull characteristically features an elon- opportunity. Derryberry et al. (2011) found constrained morpho- gated rostrum, a pair of chisel-like and ever-growing upper and logical evolution in the radiation of Furnariidae, Tran (2014) lower incisors that is separated by a diastema from a battery of detected a possible lack of ecological opportunity in the radi- cheekteeth, and enlarged masseter muscles (Korth 1994). Rodents ation of African colobine monkeys, and Zelditch et al. (2015) are widespread, abundant, and highly diversified. Nevertheless, found that geography is a very important component in the spe- the extent of morphological specializations of rodents has sel- ciation of diverse and rapidly diversifying continental squirrels. dom been explored at large taxonomic and geographic scales. At continental scales, patterns of species and morphological di- Although most rodents have generalized diets, highly specialized versification are sometimes found to be decoupled, leading, for forms, such as strict carnivores, insectivores, and herbivores, can instance, to clades with high species diversity but limited ecolog- show convergence in morphology (Samuels 2009; Rowe et al. ical variability (Kozak et al. 2006; Burbrink et al. 2012). The role 2016). The convergence of ecology and morphology is especially of ecological opportunity in continental radiations is still to be well documented for rodents living on different continents (Wood better elucidated, and requires an investigation of both ecomor- 1947; Samuels and van Valkenburgh 2008; Rodrigues et al. 2015). phological associations and temporal changes in diversity and Wood (1935, p. 250) once observed “‘Parallelism, parallelism, morphological diversification. more parallelism and still more parallelism’ is the evolutionary Temporal changes in a radiation explored via cumulative pat- motto of the rodents.” terns of lineage and morphological disparity through time (DTT) We studied one of the most impressive rodent radiations, can inform about the tempo of morphological diversification. Ra- which took place during the Neogene in the Neotropical re- diations that are considered adaptive are thought to exhibit an gion.
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