Emma E. Goldberg

Species Selection Maintains Self-Incompatibility

Incompatible Self-Compatibility Macroevolutionary processes driving species differences in diversification rates are important in explaining the variation we see in nature, but the extent of this process and how much the traits within a single species can drive changes in the diversification rate are unknown. Goldberg et al. (p. 493; see the Perspective by Wright and Barrett) analyzed the phylogenetics of the plant family Solanaceae and found that rates of extinction are greater for self-pollinating species than outbreeding species. Species-level selection against the deleterious effects of inbreeding may explain why self-fertilization, despite its short-term evolutionary advantages, has not spread to become more common in the flowering plants. Self-incompatibility in a family of plants is associated with appreciably higher rates of speciation. Identifying traits that affect rates of speciation and extinction and, hence, explain differences in species diversity among clades is a major goal of evolutionary biology. Detecting such traits is especially difficult when they undergo frequent transitions between states. Self-incompatibility, the ability of hermaphrodites to enforce outcrossing, is frequently lost in flowering plants, enabling self-fertilization. We show, however, that in the nightshade plant family (Solanaceae), species with functional self-incompatibility diversify at a significantly higher rate than those without it. The apparent short-term advantages of potentially self-fertilizing individuals are therefore offset by strong species selection, which favors obligate outcrossing.

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.

Model Inadequacy and Mistaken Inferences of Trait-Dependent Speciation

Species richness varies widely across the tree of life, and there is great interest in identifying ecological, geographic, and other factors that affect rates of species proliferation. Recent methods for explicitly modeling the relationships among character states, speciation rates, and extinction rates on phylogenetic trees- BiSSE, QuaSSE, GeoSSE, and related models-have been widely used to test hypotheses about character state-dependent diversification rates. Here, we document the disconcerting ease with which neutral traits are inferred to have statistically significant associations with speciation rate. We first demonstrate this unfortunate effect for a known model assumption violation: shifts in speciation rate associated with a character not included in the model. We further show that for many empirical phylogenies, characters simulated in the absence of state-dependent diversification exhibit an even higher Type I error rate, indicating that the method is susceptible to additional, unknown model inadequacies. For traits that evolve slowly, the root cause appears to be a statistical framework that does not require replicated shifts in character state and diversification. However, spurious associations between character state and speciation rate arise even for traits that lack phylogenetic signal, suggesting that phylogenetic pseudoreplication alone cannot fully explain the problem. The surprising severity of this phenomenon suggests that many trait-diversification relationships reported in the literature may not be real. More generally, we highlight the need for diagnosing and understanding the consequences of model inadequacy in phylogenetic comparative methods.

ON PHYLOGENETIC TESTS OF IRREVERSIBLE EVOLUTION

Abstract “Dollos law” states that, following loss, a complex trait cannot reevolve in an identical manner. Although the law has previously fallen into disrepute, it has only recently been challenged with statistical phylogenetic methods. We employ simulation studies of an irreversible binary character to show that rejections of Dollos law based on likelihood-ratio tests of transition rate constraints or on reconstructions of ancestral states are frequently incorrect. We identify two major causes of errors: incorrect assignment of root state frequencies, and neglect of the effect of the character state on rates of speciation and extinction. Our findings do not necessarily overturn the conclusions of phylogenetic studies claiming reversals, but we demonstrate devastating flaws in the methods that are the foundation of all such studies. Furthermore, we show that false rejections of Dollos law can be reduced by the use of appropriate existing models and model selection procedures. More powerful tests of irreversibility require data beyond phylogenies and character states of extant taxa, and we highlight empirical work that incorporates additional information.

TEMPO AND MODE IN PLANT BREEDING SYSTEM EVOLUTION

Classic questions about trait evolution—including the directionality of character change and its interactions with lineage diversification—intersect in the study of plant breeding systems. Transitions from self‐incompatibility to self‐compatibility are frequent, and they may proceed within a species (“anagenetic” mode of breeding system change) or in conjunction with speciation events (“cladogenetic” mode of change). We apply a recently developed phylogenetic model to the nightshade family Solanaceae, quantifying the relative contributions of these two modes of evolution along with the tempo of breeding system change, speciation, and extinction. We find that self‐incompatibility, a genetic mechanism that prevents self‐fertilization, is lost largely by the cladogenetic mode. Self‐compatible species are thus more likely to arise from the isolation of a newly self‐compatible population than from species‐wide fixation of self‐compatible mutants. Shared polymorphism at the locus that governs self‐incompatibility shows it to be ancestral and not regained within this family. We demonstrate that failing to account for cladogenetic character change misleads phylogenetic tests of evolutionary irreversibility, both for breeding system in Solanaceae and on simulated trees.

Diversity, endemism, and age distributions in macroevolutionary sources and sinks.

Quantitative tests of historical hypotheses are necessary to advance our understanding of biogeographic patterns of species distributions, but direct tests are often hampered by incomplete fossil or historical records. Here we present an alternative approach in which we develop a dynamic model that allows us to test hypotheses about regional rates of taxon origination, extinction, and dispersal using information on ages and current distributions of taxa. With this model, we test two assumptions traditionally made in the context of identifying regions as “centers of origin”—that regions with high origination rates will have high diversity and high endemism. We find that these assumptions are not necessarily valid. We also develop expressions for the regional age distributions of extant taxa and show that these may yield better insight into regional evolutionary rates. We then apply our model to data on the biogeography and ages of extant genera of marine bivalves and conclude that diversity in polar regions predominantly reflects dispersal of taxa that evolved elsewhere rather than in situ origination‐extinction dynamics.

Origins and consequences of serpentine endemism in the California flora.

Habitat specialization plays an important role in the creation and loss of biodiversity over ecological and evolutionary time scales. In California, serpentine soils have a distinctive flora, with 246 serpentine habitat specialists (i.e., endemics). Using molecular phylogenies for 23 genera containing 784 taxa and 51 endemics, we infer few transitions out of the endemic state, which is shown by an analysis of transition rates to simply reflect the low frequency of endemics (i.e., reversal rates were high). The finding of high reversal rates, but a low number of reversals, is consistent with the widely hypothesized trade‐off between serpentine tolerance and competitive ability, under which serpentine endemics are physiologically capable of growing in less‐stressful habitats but competitors lead to their extirpation. Endemism is also characterized by a decrease in speciation and extinction rates and a decrease in the overall diversification rate. We also find that tolerators (species with nonserpentine and serpentine populations) undergo speciation in serpentine habitats to give rise to new serpentine endemics but are several times more likely to lose serpentine populations to produce serpentine‐intolerant taxa. Finally, endemics were younger on average than nonendemics, but this alone does not explain their low diversification.

Origination, Extinction, and Dispersal: Integrative Models for Understanding Present‐Day Diversity Gradients*

Species diversity gradients seen today are, to a large degree, a product of history. Spatially nonrandom originations, extinctions, and changes in geographic distributions can create gradients in species and higher‐taxon richness, but the relative roles of each of these processes remain poorly documented. Existing explanations of diversity gradients have tended to focus on either macroevolutionary or biogeographic processes; integrative models that include both are largely lacking. We used simple models that incorporate origination and extinction rates along with dispersal of taxa between regions to show that dispersal not only affects regional richness patterns but also has a strong influence on the average age of taxa present in a region. Failure to take into account the effects of dispersal can, in principle, lead to biased estimates of diversification rates and potentially wrong conclusions regarding processes driving latitudinal and other gradients in diversity. Thus, it is critical to include the effects of dispersal when formulating and testing hypotheses about the causes of large‐scale gradients in diversity. Finally, the model results, in conjunction with the results of existing empirical studies, suggest that the nature of macroevolutionary and biogeographic processes may differ between terrestrial and marine diversity gradients.

Not Just a Theory—The Utility of Mathematical Models in Evolutionary Biology

Models have made numerous contributions to evolutionary biology, but misunderstandings persist regarding their purpose. By formally testing the logic of verbal hypotheses, proof-of-concept models clarify thinking, uncover hidden assumptions, and spur new directions of study. thumbnail image credit: modified from the Biodiversity Heritage Library

Species’ Borders and Dispersal Barriers

Range limits of species are determined by combined effects of physical, historical, ecological, and evolutionary forces. We consider a subset of these factors by using spatial models of competition, hybridization, and local adaptation to examine the effects of partial dispersal barriers on the locations of borders between similar species. Prompted by results from population genetic models and biogeographic observations, we investigate the conditions under which species’ borders are attracted to regions of reduced dispersal. For borders maintained by competition or hybridization, we find that dispersal barriers can attract borders whose positions would otherwise be either neutrally stable or moving across space. Borders affected strongly by local adaptation and gene flow, however, are repelled from dispersal barriers. These models illustrate how particular biotic and abiotic factors may combine to limit species’ ranges, and they help to elucidate mechanisms by which range limits of many species may coincide.