John J. Schenk

Ecological opportunity and the origin of adaptive radiations

Ecological opportunity – through entry into a new environment, the origin of a key innovation or extinction of antagonists – is widely thought to link ecological population dynamics to evolutionary diversification. The population‐level processes arising from ecological opportunity are well documented under the concept of ecological release. However, there is little consensus as to how these processes promote phenotypic diversification, rapid speciation and adaptive radiation. We propose that ecological opportunity could promote adaptive radiation by generating specific changes to the selective regimes acting on natural populations, both by relaxing effective stabilizing selection and by creating conditions that ultimately generate diversifying selection. We assess theoretical and empirical evidence for these effects of ecological opportunity and review emerging phylogenetic approaches that attempt to detect the signature of ecological opportunity across geological time. Finally, we evaluate the evidence for the evolutionary effects of ecological opportunity in the diversification of Caribbean Anolis lizards. Some of the processes that could link ecological opportunity to adaptive radiation are well documented, but others remain unsupported. We suggest that more study is required to characterize the form of natural selection acting on natural populations and to better describe the relationship between ecological opportunity and speciation rates.

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.

Effects of Substitution Models on Divergence Time Estimates: Simulations and an Empirical Study of Model Uncertainty using Cornales

Abstract Phylogenetic divergence time estimates inferred from trees optimized using maximum likelihood apply branch lengths. These branch lengths are influenced by the substitution model applied in the analysis, which can, in turn, affect divergence time estimates. To examine the effects of substitution models on divergence time estimates, we applied an empirical data set for Cornales that had 16 calibration point constraints in maximum likelihood analyses using 19 different substitution models to obtain topologies with branch lengths. Penalized likelihood was then used to obtain divergence time estimates for corresponding nodes of these topologies. Discrepancy in divergence time estimates among corresponding nodes of trees constructed with different models was small in most cases (falling within 95% confidence intervals based on the most supported model); however, we recovered instances of nodes differing by as much as 23.7% from times on corresponding nodes of the phylogeny reconstructed from our best-fit substitution model. We estimated that, on average for all nodes within a tree, divergence times differ 1.0–3.6% among the trees based on different models; however, the range of variation differs greatly among trees based on different substitution models. Discrepancy in divergence time estimates was associated with long branches, although using models similar to the best-fit model reduced this. Branches of a length within one standard deviation of mean branch lengths were an unexpected source of discrepancy regardless of the substitution model applied, although the cause of this discrepancy was unclear. We found no differences in disparity among nodes that were reconstructed in deep-, mid, or shallow-level regions of the topologies. Simulations demonstrated that use of underparameterized models affected age estimates more than use of overparameterized models. Increasing the number of calibration points can limit but not completely remove discrepancies introduced by underparameterized models.

Muroid rodent phylogenetics: 900-species tree reveals increasing diversification rates

We combined new sequence data for more than 300 muroid rodent species with our previously published sequences for up to five nuclear and one mitochondrial genes to generate the most widely and densely sampled hypothesis of evolutionary relationships across Muroidea. An exhaustive screening procedure for publically available sequences was implemented to avoid the propagation of taxonomic errors that are common to supermatrix studies. The combined data set of carefully screened sequences derived from all available sequences on GenBank with our new data resulted in a robust maximum likelihood phylogeny for 900 of the approximately 1,620 muroids. Several regions that were equivocally resolved in previous studies are now more decisively resolved, and we estimated a chronogram using 28 fossil calibrations for the most integrated age and topological estimates to date. The results were used to update muroid classification and highlight questions needing additional data. We also compared the results of multigene supermatrix studies like this one with the principal published supertrees and concluded that the latter are unreliable for any comparative study in muroids. In addition, we explored diversification patterns as an explanation for why muroid rodents represent one of the most species-rich groups of mammals by detecting evidence for increasing net diversification rates through time across the muroid tree. We suggest the observation of increasing rates may be due to a combination of parallel increases in rate across clades and high average extinction rates. Five increased diversification-rate-shifts were inferred, suggesting that multiple, but perhaps not independent, events have led to the remarkable species diversity in the superfamily. Our results provide a phylogenetic framework for comparative studies that is not highly dependent upon the signal from any one gene.

Evolution of limited seed dispersal ability on gypsum islands

UNLABELLED PREMISE OF THE STUDY Dispersal is a major feature of plant evolution that has many advantages but is not always favored. Wide dispersal, for example, leads to greater seed loss in oceanic-island endemics, and evolution has favored morphologies that limit dispersal. I tested the hypothesis that selection favored limited dispersal on gypsum islands in western North America, where edaphic communities are sparsely vegetated except for a specialized flora that competes poorly with the surrounding flora. • METHODS I applied a series of comparative phylogenetic approaches to gypsophilic species of Mentzelia section Bartonia (Loasaceae) to investigate the evolution of limited dispersal function in seed wings, which increase primary dispersal by wind. Through these tests, I determined whether narrowed wings were selected for in gypsophilic species. • KEY RESULTS Gypsophily was derived four to seven times. Seed area was not significantly correlated with gypsophily or wing area. Wing area was significantly smaller in the derived gypsum endemics, supporting the hypothesis in favor of limited dispersal function. A model-fitting approach identified two trait optima in wing area, with gypsum endemics having a lower optimum. • CONCLUSIONS Evolution into novel ecologies influences morphological evolution. Morphological characters have been selected for limited dispersal following evolution onto gypsum islands. Selection for limited dispersal ability has occurred across animals and plants, both in oceanic and terrestrial systems, which suggests that reduced dispersal ability may be a general process: selection favors limited dispersal if the difference in survival between the habitat of the parent and the surrounding area is great enough.

Describing a New Species into a Polyphyletic Genus: Taxonomic Novelty in Ledermanniella s.l. (Podostemaceae) from Cameroon

Abstract Ledermanniella s.l. (Podostemaceae) occurs in western Africa, where species are commonly localized to single rapids or waterfalls. Recent collecting efforts in this region have led to the discovery of new species diversity; however, molecular phylogenetic analyses estimate the genus as polyphyletic and associated with at least nine other genera. Here, we describe a new species of Ledermanniella s.l. while addressing the problem of describing a species into a polyphyletic genus with a phylogenetic approach. We sampled species diversity for molecular and morphological data and combined them with morphological data only from the new species, which we were unable to sequence because of non-optimal DNA preservation or other reasons. We tested and rejected the monophyly of Ledermanniella s.l. and L. subgenus Ledermanniella with the Shimodaira-Hasegawa test, and found support for a monophyletic L. subgenus Phyllosoma, which was recently treated at the genus level as Inversodicraea. Based on Bayesian phylogenetic inference, we describe Inversodicraea achoundongii, which we infer in a clade with I. cristata, I. ntemensis (combined here), and I. annithomae. The morphological and phylogenetic consequences of these results are discussed, including leaf homologies, along with a description of the ecological, distributional, and conservation implications of the new species and western African Ledermanniella s.l.

Phylogeny and Taxonomy of Mentzelia Section Bartonia (Loasaceae)

Abstract Taxonomic problems in Mentzelia section Bartonia (Loasaceae) are addressed using phylogeny reconstructions based on nuclear ribosomal DNA sequences from the ITS and ETS regions. Our results indicate sect. Bartonia is monophyletic and consists of two well-supported, species-rich clades. One of these two deepest clades consists of the Great Plains M. decapetala and a group of species centered in the North American intermountain region that have been described as subshrubby; whereas, the second deepest clade is more widespread and includes taxa from the Chihuahuan and Sonoran deserts as well as the Great Plains, Rocky Mountains, and intermountain region. Hypothesis tests applying the Shimodaira-Hasegawa (SH) test and Bayes factors (BF) rejected unequivocally the monophyly of (1) the ‘subshrubby’ group, suggesting multiple origins of the ‘subshrubby’ form; (2) M. multicaulis s. l., which consists of disparate clades we propose as separate species; and (3) M. multiflora s. l., which was recovered as highly polyphyletic. Hypothesis tests were equivocal, however, in regard to the monophyly of (1) M. marginata, M. paradoxensis, and M. cronquistii; (2) M. oreophila s. l.; and (3) M. pumila s. l. We suggest following narrow taxonomic approaches to the circumscriptions of M. multicaulis, M. multiflora, and M. pumila and advocate further studies of M. oreophila and the complex including of M. marginata, M. paradoxensis, and M. cronquistii. Our results provide the most comprehensive phylogenetic hypothesis of sect. Bartonia to date, however, more variable markers will be needed to resolve a well supported phylogeny.

TAXONOMIC NOVELTIES FROM WESTERN NORTH AMERICA IN MENTZELIA SECTION BARTONIA (LOASACEAE)

Abstract Recent field collections and surveys of herbarium specimens have raised concerns about species circumscriptions and recovered several morphologically distinct populations in Mentzelia section Bartonia (Loasaceae). From the Colorado Plateau, we name M. paradoxensis from Paradox and Gypsum valleys of western Colorado, which is closely related to M. marginata. We name M. holmgreniorum from northeastern Arizona and M. filifolia from the northern border region of Arizona and New Mexico, both of which share morphological similarities with M. lagarosa, M. laciniata, and M. conspicua. From north central New Mexico, we name M. sivinskii, which is most closely related to M. procera and M. integra. We describe three varieties of M. longiloba, including M. longiloba var. yavapaiensis, which is distributed throughout Arizona, M. longiloba var. pinacatensis, which is narrowly distributed in the Pinacate Desert of Sonora, Mexico, and the northern Chihuahuan Desert M. longiloba var. chihuahuaensis. We propose the new combinations M. lagarosa and M. procera to alleviate the polyphyly of M. pumila.

The Role of Geography in Adaptive Radiation

Although the importance of biogeography in the speciation process is well recognized, the fundamental role of geographic diversification during adaptive radiations has not been studied to determine its importance during the adaptive radiation process. We examined the relationship between lineage and regional diversification patterns in the South American rodent subfamily Sigmodontinae, one of the best candidates for an adaptive radiation in mammals, to propose a conceptual framework for geographic transitions during adaptive radiations. We reconstructed a time-calibrated phylogeny from four nuclear genes and one mitochondrial gene for 77% of sigmodontine diversity. Historical biogeography was reconstructed among 14 regions, for which we applied a sliding-window approach to estimate regional transition rates through time. We compared these rate patterns and measured whether regions consisted of species that were more phylogenetically related than expected by chance. Following the initial South American colonization around 7 million years ago, multiple expansions from northern regions correlated with a burst of speciation. Subsequently, both diversification and regional transition rates decreased overall and within the majority of regions. Despite high regional transition rates, nearly all regional assemblages were phylogenetically clustered, indicating that within-region diversification was common. We conclude that biogeographic complexity and partitioning played a profound role in the adaptive radiation of the South American Sigmodontinae (Oryzomyalia), the degree to which is determined by the relative scales of spatial variation and dispersal abilities.

Mentzelia canyonensis (Loasaceae), a new species endemic to the Grand Canyon, Arizona, U.S.A.

We describe Mentzelia canyonensis, a new species endemic to the Grand Canyon. Based on floral and fruit forms, shoot system architecture, and phylogenetic analyses of nuclear ribosomal DNA, we infer that M. canyonensis belongs to the ‘subshrubby’ clade of Mentzelia section Bartonia, which includes the morphologically similar M. hualapaiensis, M. oreophila, M. puberula, and M. tiehmii. The new species is most similar to M. hualapaiensis, which is also known only from the Grand Canyon. These two species share leaf shape, subshrubby habits, corolla color, and fruit shape, although they differ in staminode presence and especially in leaf and corolla size. Principal component analyses of variation among floral and vegetative traits demonstrates that M. canyonensis and M. hualapaiensis share highly overlapping floral character space, but M. canyonensis occupies unique vegetative character space compared to similar species. A dichotomous key is provided to assist with identification of, and differentiation among, species of Mentzelia section Bartonia that occur in the Grand Canyon region.