Plant traits-the morphological, anatomical, physiological, biochemical and phenological characteristics of plants-determine how plants respond to environmental factors, affect other trophic levels, and influence ecosystem properties and their benefits and detriments to people. Plant trait data thus represent the basis for a vast area of research spanning from evolutionary biology, community and functional ecology, to biodiversity conservation, ecosystem and landscape management, restoration, biogeography and earth system modelling. Since its foundation in 2007, the TRY database of plant traits has grown continuously. It now provides unprecedented data coverage under an open access data policy and is the main plant trait database used by the research community worldwide. Increasingly, the TRY database also supports new frontiers of trait-based plant research, including the identification of data gaps and the subsequent mobilization or measurement of new data. To support this development, in this article we evaluate the extent of the trait data compiled in TRY and analyse emerging patterns of data coverage and representativeness. Best species coverage is achieved for categorical traits-almost complete coverage for 'plant growth form'. However, most traits relevant for ecology and vegetation modelling are characterized by continuous intraspecific variation and trait-environmental relationships. These traits have to be measured on individual plants in their respective environment. Despite unprecedented data coverage, we observe a humbling lack of completeness and representativeness of these continuous traits in many aspects.We, therefore, conclude that reducing data gaps and biases in the TRY database remains a key challenge and requires a coordinated approach to data mobilization and trait measurements. This can only be achieved in collaboration with other initiatives. Geosphere-Biosphere Program (IGBP) and DIVERSITAS, the TRY database (TRY-not an acronym, rather a statement of sentiment; https ://www.try-db.org; Kattge et al., 2011) was proposed with the explicit assignment to improve the availability and accessibility of plant trait data for ecology and earth system sciences. The Max Planck Institute for Biogeochemistry (MPI-BGC) offered to host the database and the different groups joined forces for this community-driven program. Two factors were key to the success of TRY: the support and trust of leaders in the field of functional plant ecology submitting large databases and the long-term funding by the Max Planck Society, the MPI-BGC and the German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, which has enabled the continuous development of the TRY database.
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.
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.
T2-type RNases are responsible for self-pollen recognition and rejection in three distantly related families of flowering plantsthe 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 Ϸ75% of dicot families, our results indicate that RNase-based self-incompatibility was the ancestral state in the majority of dicots. M ultiallelic self-incompatibility systems prevent selffertilization in many flowering plants. The molecular bases of self-incompatibility in three angiosperm families-the Brassicaceae, Papaveraceae, and Solanaceae-are all different (1-3), contradicting early speculation (4) that all self-incompatibility systems have a single origin. Nevertheless, three distantly related families-the Solanaceae, Scrophulariaceae, and Rosaceaeuse T2-type RNases as the mechanism of self-pollen recognition and rejection (5-7). In this study we use an extensive plant T2-RNase database to determine whether use of selfincompatibility RNases (S-RNases) in these families is homologous or convergent.The Solanaceae and Scrophulariaceae belong to the subclass Asteridae whereas the Roasaceae are in the subclass Rosidae (Fig. 1). Homology of S-RNases would suggest that RNase-based gametophytic self-incompatibility (GSI) was present in the common ancestor of these subclasses, which together comprise roughly three-quarters of dicot families (8, 9). Moreover, a single origin would imply rampant losses of RNase-based GSI and several gains of other forms of incompatibility among higher dicots. Alternatively, polyphyletic relationships of extant SRNases would represent a spectacular example of functional convergence.Estimating the evolutionary relationships among S-RNases is difficult for several reasons. First, T2-type RNases are relatively short (Ϸ650 bp of coding sequence), potentially providing limited information on relationships. Second, the time since divergence of the subclasses Asteridae and Rosidae is quite long, perhaps 110 million years (10). Finally, the strong negative frequency-dependent selection that operates on the S-locus is expected to cause extensive sequence divergence once the system originates (11). Thus, even if S-RNases arose separately in different groups, phylogenetic reconstructions might tend to unite them due to long-branch attraction (12), the tendency for methods of phylogenetic reconstruction to unite rapidly evolving taxa because of random...
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. K E Y W O R D S :Comparative methods, Dollo's law, macroevolution, self-incompatibility, Solanaceae.
386I.387II.388III.390IV.393V.394395References395 Summary A compound hypothesis positing that self‐fertilization is an evolutionary dead end conflates two distinct claims: the transition from outcrossing to selfing is unidirectional; and the diversification rate, or the balance of the speciation and extinction rate, is negative for selfing species. Both claims have enjoyed widespread informal support for decades, but have recently come under suspicion. Sources of data that apparently contradict strongly asymmetric mating system transitions often rely on statistical phylogenetic tests plagued by profound flaws. Although recently developed models mend preceding approaches, they have been employed sparingly, and many problems remain. Theoretical investigations, genetic data and applications of new phylogenetic methods provide indirect support for an association of selfing with negative diversification rates. We lack direct tests of reversals from selfing to outcrossing, and require data concerning the genetic basis and complexity of independently evolved outcrossing adaptations. The identification of the mechanisms that limit the longevity of selfing lineages has been difficult. Limitations may include brief and variable durations of selfing lineages, as well as ongoing difficulties in relating additive genetic and nucleotide variation. Furthermore, a common line of evidence for the stability of mixed mating – based simply on its frequent occurrence – is misleading. We make specific suggestions for research programs that aim to provide a richer understanding of mating system evolution and seriously challenge Stebbins’ venerable hypothesis.
Loss of complex characters is thought to be irreversible (Dollo's 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 Dollo's law.ancestral state reconstruction ͉ breeding system evolution ͉ self-compatibility ͉ self-incompatibility ͉ Solanaceae I n hermaphroditic plants, obligate outcrossing is often enforced by self-incompatibility (SI), a genetic mechanism for recognition and rejection of a plant's own pollen. In the plant families Solanaceae, Scrophulariaceae s.l., and Rosaceae, the recognition of self-pollen by the plant's female organs is mediated by ribonucleases (1-3) produced by the SI locus (S-locus). Empirical studies have found that alleles at the S-locus [SI alleles (S-alleles)] are highly polymorphic (often Ͻ50% amino acid identity), and that dozens are maintained at the S-locus within populations and species (4). Extreme polymorphism results from rare allele advantage, a feature common to other selfrecognition loci such as the major histocompatibility complex loci in jawed vertebrates and SI loci in fungi (5, 6).The selective basis favoring rare alleles in plant SI systems is simple. If an allele in the haploid pollen matches either allele expressed by the diploid style, fertilization is prevented. Therefore, plants with rare alleles have more available mates, and those with common alleles fewer. The result of this form of selection is striking polymorphism that persists for tens of millions of years (7,8). Many allele lineages are older than the genera that contain them (7-10). For example, it is common for a Peruvian tomato (Solanum peruvianum) allele to be more closely related to an allele from a wild tobacco (Nicotiana alata) than to any other Peruvian tomato allele, even though these species diverged Ϸ30 million years ago (7). The observation of allele polymorphism shared among extant SI species provides strong evidence that this polymorphism was present in their comm...
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