Boris Igic

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.

LOSS OF SELF-INCOMPATIBILITY AND ITS EVOLUTIONARY CONSEQUENCES

We review and analyze the available literature on the frequency and distribution of self‐incompatibility (SI) among angiosperms and find that SI is reported in more than 100 families and occurs in an estimated 39% of species. SI frequently has been lost but rarely has been gained during angiosperm diversification, and there is no evidence that any particular system of SI, once lost, has been regained. Irreversible loss of SI systems is thought to occur because transitions to self‐compatibility (SC) are accompanied by collapse of variation at the S‐locus and by accumulation of loss‐of‐function mutations at multiple loci involved in the incompatibility response. The asymmetry in transitions implies either that SI is declining in frequency or that it provides a macroevolutionary advantage. We present a model in which the loss of SI is irreversible and species can be SI, SC but outcrossing, or predominantly selfing. Increased diversification rates of SI relative to SC taxa are required to maintain SI at equilibrium, while transition rates between states, together with state‐specific diversification rates, govern the frequency distribution of breeding‐system states. We review empirical studies about the causes and consequences of the loss of SI, paying particular attention to the model systems Arabidopsis and Solanum sect. Lycopersicon. In both groups, losses of SI have been recent and were accompanied by loss of most or all of the functional variation at the S‐locus. Multiple loss‐of‐function mutations are commonly found. Some evidence indicates that mutations causing SC strongly increase the selfing rate and that SC species have lower genetic diversity than their SI relatives, perhaps causing an increase in the extinction rate.

Evolutionary relationships among self-incompatibility RNases.

T2-type RNases are responsible for self-pollen recognition and rejection in three distantly related families of flowering plants—the Solanaceae, Scrophulariaceae, and Rosaceae. We used phylogenetic analyses of 67 T2-type RNases together with information on intron number and position to determine whether the use of RNases for self-incompatibility in these families is homologous or convergent. All methods of phylogenetic reconstruction as well as patterns of variation in intron structure find that all self-incompatibility RNases along with non-S genes from only two taxa form a monophyletic clade. Several lines of evidence suggest that the best interpretation of this pattern is homology of self-incompatibility RNases from the Scrophulariaceae, Solanaceae, and Rosaceae. Because the most recent common ancestor of these three families is the ancestor of ≈75% of dicot families, our results indicate that RNase-based self-incompatibility was the ancestral state in the majority of dicots.

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.

Ancient polymorphism reveals unidirectional breeding system shifts

Loss of complex characters is thought to be irreversible (Dollos law). However, hypotheses of irreversible evolution are remarkably difficult to test, especially when character transitions are frequent. In such cases, inference of ancestral states, in the absence of fossil evidence, is uncertain and represents the single greatest constraint for reconstructing the evolutionary history of characters. Breeding system character transitions are of particular interest because they affect the amount and distribution of genetic variation within species. Transitions from obligate outcrossing to partial or predominant self-fertilization are thought to represent one of the most common trends in flowering plants. We use the unique molecular genetic properties (manifested as deep persistent polymorphisms) of the locus that enforces outcrossing to demonstrate that its loss is irreversible in the plant family Solanaceae. We argue that current phylogenetic methods of reconstruction are potentially inadequate in cases where ancestral state information is inferred by using only the phylogeny and the distribution of character states in extant taxa. This study shows in a statistical framework that a particular character transition is irreversible, consistent with Dollos law.

Primary structural features of the S haplotype-specific F-box protein, SFB, in Prunus

The gene SFB encodes an F-box protein that has appropriate S-haplotype-specific variation to be the pollen determinant in the S-RNase-based gametophytic self-incompatibility (GSI) reaction in Prunus (Rosaceae). To further characterize Prunus SFB, we cloned and sequenced four additional alleles from sweet cherry (P. avium), SFB1, SFB2, SFB4, and SFB5. These four alleles showed haplotype-specific sequence diversity similar to the other nine SFB alleles that have been cloned. In an amino acid alignment of Prunus SFBs, including the four newly cloned alleles, 121 out of the 384 sites were conserved and an additional 65 sites had only conservative replacements. Amino acid identity among the SFBs ranged from 66.0% to 82.5%. Based on normed variability indices (NVI), 34 of the non-conserved sites were considered to be highly variable. Most of the variable sites were located at the C-terminal region. A window-averaged plot of NVI indicated that there were two variable and two hypervariable regions. These variable and hypervariable regions appeared to be hydrophilic or at least not strongly hydrophobic, which suggests that these regions may be exposed on the surface and function in the allele specificity of the GSI reaction. Evidence of positive selection was detected using maximum likelihood methods with sites under positive selection concentrated in the variable and hypervariable regions.

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.

THE DISTRIBUTION OF PLANT MATING SYSTEMS: STUDY BIAS AGAINST OBLIGATELY OUTCROSSING SPECIES

Abstract Early models of plant mating-system evolution argued that predominant outcrossing and selfing are alternative stable states. At least for animal-pollinated species, recent summaries of empirical studies have suggested the opposite—that outcrossing rates do not show the expected bimodal distribution. However, it is generally accepted that several potential biases can affect conclusions from surveys of published outcrossing rates. Here, we examine one potential bias and find that published studies of outcrossing rates contain far fewer obligate outcrossers than expected. We approximate the magnitude of this study bias and present the distribution of outcrossing rates after compensating for it. Because this study examines only one potential bias, and finds it to be large, conclusions regarding either the frequency of mixed mating or the shape of the distribution of outcrossing rates in nature are premature.

The scope of Baker's law

Bakers law refers to the tendency for species that establish on islands by long-distance dispersal to show an increased capacity for self-fertilization because of the advantage of self-compatibility when colonizing new habitat. Despite its intuitive appeal and broad empirical support, it has received substantial criticism over the years since it was proclaimed in the 1950s, not least because it seemed to be contradicted by the high frequency of dioecy on islands. Recent theoretical work has again questioned the generality and scope of Bakers law. Here, we attempt to discern where the idea is useful to apply and where it is not. We conclude that several of the perceived problems with Bakers law fall away when a narrower perspective is adopted on how it should be circumscribed. We emphasize that Bakers law should be read in terms of an enrichment of a capacity for uniparental reproduction in colonizing situations, rather than of high selfing rates. We suggest that Bakers law might be tested in four different contexts, which set the breadth of its scope: the colonization of oceanic islands, metapopulation dynamics with recurrent colonization, range expansions with recurrent colonization, and colonization through species invasions.

A 15-Myr-Old Genetic Bottleneck

Balancing selection preserves variation at the self-incompatibility locus (S-locus) of flowering plants for tens of millions of years, making it possible to detect demographic events that occurred prior to the origin of extant species. In contrast to other Solanaceae examined, SI species in the sister genera Physalis and Witheringia share restricted variation at the S-locus. This restriction is indicative of an ancient bottleneck that occurred in a common ancestor. We sequenced 14 S-alleles from the subtribe Iochrominae, a group that is sister to the clade containing Physalis and Witheringia. At least 6 ancient S-allele lineages are represented among these alleles, demonstrating that the Iochrominae taxa do not share the restriction in S-locus diversity. Therefore, the bottleneck occurred after the divergence of the Iochrominae from the lineage leading to the most recent common ancestor of Physalis and Witheringia. Using cpDNA sequences, 3 fossil dates, and a Bayesian-relaxed molecular clock approach, the crown group of Solanaceae was estimated to be 51 Myr old and the restriction of variation at the S-locus occurred 14.0-18.4 Myr before present. These results confirm the great age of polymorphism at the S-locus and the utility of loci under balancing selection for deep historical inference.