Richard H. Ree

Maximum Likelihood Inference of Geographic Range Evolution by Dispersal, Local Extinction, and Cladogenesis

In historical biogeography, model-based inference methods for reconstructing the evolution of geographic ranges on phylogenetic trees are poorly developed relative to the diversity of analogous methods available for inferring character evolution. We attempt to rectify this deficiency by constructing a dispersal-extinction-cladogenesis (DEC) model for geographic range evolution that specifies instantaneous transition rates between discrete states (ranges) along phylogenetic branches and apply it to estimating likelihoods of ancestral states (range inheritance scenarios) at cladogenesis events. Unlike an earlier version of this approach, the present model allows for an analytical solution to probabilities of range transitions as a function of time, enabling free parameters in the model, rates of dispersal, and local extinction to be estimated by maximum likelihood. Simulation results indicate that accurate parameter estimates may be difficult to obtain in practice but also show that ancestral range inheritance scenarios nevertheless can be correctly recovered with high success if rates of range evolution are low relative to the rate of cladogenesis. We apply the DEC model to a previously published, exemplary case study of island biogeography involving Hawaiian endemic angiosperms in Psychotria (Rubiaceae), showing how the DEC model can be iteratively refined from inspecting inferences of range evolution and also how geological constraints involving times of island origin may be imposed on the likelihood function. The DEC model is sufficiently similar to character models that it might serve as a gateway through which many existing comparative methods for characters could be imported into the realm of historical biogeography; moreover, it might also inspire the conceptual expansion of character models toward inclusion of evolutionary change as directly coincident, either as cause or consequence, with cladogenesis events. The DEC model is thus an incremental advance that highlights considerable potential in the nascent field of model-based historical biogeographic inference.

A LIKELIHOOD FRAMEWORK FOR INFERRING THE EVOLUTION OF GEOGRAPHIC RANGE ON PHYLOGENETIC TREES

Abstract At a time when historical biogeography appears to be again expanding its scope after a period of focusing primarily on discerning area relationships using cladograms, new inference methods are needed to bring more kinds of data to bear on questions about the geographic history of lineages. Here we describe a likelihood framework for inferring the evolution of geographic range on phylogenies that models lineage dispersal and local extinction in a set of discrete areas as stochastic events in continuous time. Unlike existing methods for estimating ancestral areas, such as dispersal‐vicariance analysis, this approach incorporates information on the timing of both lineage divergences and the availability of connections between areas (dispersal routes). Monte Carlo methods are used to estimate branch‐specific transition probabilities for geographic ranges, enabling the likelihood of the data (observed species distributions) to be evaluated for a given phylogeny and parameterized paleogeographic model. We demonstrate how the method can be used to address two biogeographic questions: What were the ancestral geographic ranges on a phylogenetic tree? How were those ancestral ranges affected by speciation and inherited by the daughter lineages at cladogenesis events? For illustration we use hypothetical examples and an analysis of a Northern Hemisphere plant clade (Cercis), comparing and contrasting inferences to those obtained from dispersal‐vicariance analysis. Although the particular model we implement is somewhat simplistic, the framework itself is flexible and could readily be modified to incorporate additional sources of information and also be extended to address other aspects of historical biogeography.

Plant mating systems in a changing world

There is increasing evidence that human disturbance can negatively impact plant-pollinator interactions such as outcross pollination. We present a meta-analysis of 22 studies involving 27 plant species showing a significant reduction in the proportion of seeds outcrossed in response to anthropogenic habitat modifications. We discuss the evolutionary consequences of disturbance on plant mating systems, and in particular whether reproductive assurance through selfing effectively compensates for reduced outcrossing. The extent to which disturbance reduces pollinator versus mate availability could generate diverse selective forces on reproductive traits. Investigating how anthropogenic change influences plant mating will lead to new opportunities for better understanding of how mating systems evolve, as well as of the ecological and evolutionary consequences of human activities and how to mitigate them.

Inferring Phylogeny and Introgression using RADseq Data: An Example from Flowering Plants (Pedicularis: Orobanchaceae)

Phylogenetic relationships among recently diverged species are often difficult to resolve due to insufficient phylogenetic signal in available markers and/or conflict among gene trees. Here we explore the use of reduced-representation genome sequencing, specifically in the form of restriction-site associated DNA (RAD), for phylogenetic inference and the detection of ancestral hybridization in non-model organisms. As a case study, we investigate Pedicularis section Cyathophora, a systematically recalcitrant clade of flowering plants in the broomrape family (Orobanchaceae). Two methods of phylogenetic inference, maximum likelihood and Bayesian concordance, were applied to data sets that included as many as 40,000 RAD loci. Both methods yielded similar topologies that included two major clades: a “rex-thamnophila” clade, composed of two species and several subspecies with relatively low floral diversity, and geographically widespread distributions at lower elevations, and a “superba” clade, composed of three species characterized by relatively high floral diversity and isolated geographic distributions at higher elevations. Levels of molecular divergence between subspecies in the rex-thamnophila clade are similar to those between species in the superba clade. Using Patterson’s D-statistic test, including a novel extension of the method that enables finer-grained resolution of introgression among multiple candidate taxa by removing the effect of their shared ancestry, we detect significant introgression among nearly all taxa in the rex-thamnophila clade, but not between clades or among taxa within the superba clade. These results suggest an important role for geographic isolation in the emergence of species barriers, by facilitating local adaptation and differentiation in the absence of homogenizing gene flow. [Concordance factors; genotyping-by-sequencing; hybridization; partitioned D-statistic test; Pedicularis; restriction-site associated DNA.]

Phylogenetic Inference of Reciprocal Effects between Geographic Range Evolution and Diversification

Geographic characters--traits describing the spatial distribution of a species-may both affect and be affected by processes associated with lineage birth and death. This is potentially confounding to comparative analyses of species distributions because current models do not allow reciprocal interactions between the evolution of ranges and the growth of phylogenetic trees. Here, we introduce a likelihood-based approach to estimating region-dependent rates of speciation, extinction, and range evolution from a phylogeny, using a new model in which these processes are interdependent. We demonstrate the method with simulation tests that accurately recover parameters relating to the mode of speciation and source-sink dynamics. We then apply it to the evolution of habitat occupancy in Californian plant communities, where we find higher rates of speciation in chaparral than in forests and evidence for expanding habitat tolerances.

Amazonian Amphibian Diversity Is Primarily Derived from Late Miocene Andean Lineages

The Neotropics contains half of remaining rainforests and Earths largest reservoir of amphibian biodiversity. However, determinants of Neotropical biodiversity (i.e., vicariance, dispersals, extinctions, and radiations) earlier than the Quaternary are largely unstudied. Using a novel method of ancestral area reconstruction and relaxed Bayesian clock analyses, we reconstructed the biogeography of the poison frog clade (Dendrobatidae). We rejected an Amazonian center-of-origin in favor of a complex connectivity model expanding over the Neotropics. We inferred 14 dispersals into and 18 out of Amazonia to adjacent regions; the Andes were the major source of dispersals into Amazonia. We found three episodes of lineage dispersal with two interleaved periods of vicariant events between South and Central America. During the late Miocene, Amazonian, and Central American-Chocoan lineages significantly increased their diversity compared to the Andean and Guianan-Venezuelan-Brazilian Shield counterparts. Significant percentage of dendrobatid diversity in Amazonia and Chocó resulted from repeated immigrations, with radiations at <10.0 million years ago (MYA), rather than in situ diversification. In contrast, the Andes, Venezuelan Highlands, and Guiana Shield have undergone extended in situ diversification at near constant rate since the Oligocene. The effects of Miocene paleogeographic events on Neotropical diversification dynamics provided the framework under which Quaternary patterns of endemism evolved.

Inferring Phylogenies from RAD Sequence Data

Reduced-representation genome sequencing represents a new source of data for systematics, and its potential utility in interspecific phylogeny reconstruction has not yet been explored. One approach that seems especially promising is the use of inexpensive short-read technologies (e.g., Illumina, SOLiD) to sequence restriction-site associated DNA (RAD) – the regions of the genome that flank the recognition sites of restriction enzymes. In this study, we simulated the collection of RAD sequences from sequenced genomes of different taxa (Drosophila, mammals, and yeasts) and developed a proof-of-concept workflow to test whether informative data could be extracted and used to accurately reconstruct “known” phylogenies of species within each group. The workflow consists of three basic steps: first, sequences are clustered by similarity to estimate orthology; second, clusters are filtered by taxonomic coverage; and third, they are aligned and concatenated for “total evidence” phylogenetic analysis. We evaluated the performance of clustering and filtering parameters by comparing the resulting topologies with well-supported reference trees and we were able to identify conditions under which the reference tree was inferred with high support. For Drosophila, whole genome alignments allowed us to directly evaluate which parameters most consistently recovered orthologous sequences. For the parameter ranges explored, we recovered the best results at the low ends of sequence similarity and taxonomic representation of loci; these generated the largest supermatrices with the highest proportion of missing data. Applications of the method to mammals and yeasts were less successful, which we suggest may be due partly to their much deeper evolutionary divergence times compared to Drosophila (crown ages of approximately 100 and 300 versus 60 Mya, respectively). RAD sequences thus appear to hold promise for reconstructing phylogenetic relationships in younger clades in which sufficient numbers of orthologous restriction sites are retained across species.

Phylogeny and the evolution of flower symmetry in the Asteridae

Abstract Phylogenetic trees imply that flowers with a single plane of symmetry (zygomorphic flowers) have evolved several times independently from radially symmetrical (actinomorphic) ancestors within the Asteridae. However, there also appear to have been reversals to actinomorphy. A few evolutionarily derived actinomorphic flowers resemble mutants caused by loss-of-function mutations in genes such as CYCLOIDEA . However, a majority of the shifts from zygomorphy to actinomorphy appear to have entailed a reduction in petal number and flower size, implying a mechanism other than loss of CYCLOIDEA function. Within the Asteridae there appear to be three common forms of zygomorphy. An explanation for the virtual absence of other forms rests on the near universality of the basic orientation of the flower in the Asteridae.

Evidence for a Time‐Integrated Species‐Area Effect on the Latitudinal Gradient in Tree Diversity

The greater area of tropical forest biomes has been proposed as a factor that drives the latitudinal gradient in species diversity by modulating speciation and extinction rates. But speciation and extinction are processes that operate over millions of years, so an adequate test of area’s contribution to diversity patterns must take into consideration that biome areas have changed through time in response to climate. Here we correlate estimates of current tree species diversity with a composite parameter integrating area over geological time for each continent’s tropical, temperate, and boreal biomes. We find significant positive correlations between current tree diversity and area‐time for periods since the Eocene, Oligocene, and Miocene, which we take as evidence for a time‐integrated species‐area effect on current patterns of species richness across biomes. These results contribute to explanations for why most lineages have tropical origins and why tropical forests are more diverse than extratropical forests.

Correlated evolution of mating system and floral display traits in flowering plants and its implications for the distribution of mating system variation

Reduced allocation to structures for pollinator attraction is predicted in selfing species. We explored the association between outcrossing and floral display in a broad sample of angiosperms. We used the demonstrated relationship to test for bias against selfing species in the outcrossing rate distribution, the shape of which has relevance for the stability of mixed mating. Relationships between outcrossing rate, flower size, flower number and floral display, measured as the product of flower size and number, were examined using phylogenetically independent contrasts. The distribution of floral displays among species in the outcrossing rate database was compared with that of a random sample of the same flora. The outcrossing rate was positively associated with the product of flower size and number; individually, components of display were less strongly related to outcrossing. Compared with a random sample, species in the outcrossing rate database showed a deficit of small floral display sizes. We found broad support for reduced allocation to attraction in selfing species. We suggest that covariation between mating systems and total allocation to attraction can explain the deviation from expected trade-offs between flower size and number. Our results suggest a bias against estimating outcrossing rates in the lower half of the distribution, but not specifically against highly selfing species.