COMPARATIVE EVIDENCE FOR THE CORRELATED EVOLUTION OF POLYPLOIDY AND SELF‐COMPATIBILITY IN SOLANACEAE

Breakdown of self‐incompatibility occurs repeatedly in flowering plants with important evolutionary consequences. In plant families in which self‐incompatibility is mediated by S‐RNases, previous evidence suggests that polyploidy may often directly cause self‐compatibility through the formation of diploid pollen grains. We use three approaches to examine relationships between self‐incompatibility and ploidy. First, we test whether evolution of self‐compatibility and polyploidy is correlated in the nightshade family (Solanaceae), and find the expected close association between polyploidy and self‐compatibility. Second, we compare the rate of breakdown of self‐incompatibility in the absence of polyploidy against the rate of breakdown that arises as a byproduct of polyploidization, and we find the former to be greater. Third, we apply a novel extension to these methods to show that the relative magnitudes of the macroevolutionary pathways leading to self‐compatible polyploids are time dependent. Over small time intervals, the direct pathway from self‐incompatible diploids is dominant, whereas the pathway through self‐compatible diploids prevails over longer time scales. This pathway analysis is broadly applicable to models of character evolution in which sequential combinations of rates are compared. Finally, given the strong evidence for both irreversibility of the loss of self‐incompatibility in the family and the significant association between self‐compatibility and polyploidy, we argue that ancient polyploidy is highly unlikely to have occurred within the Solanaceae, contrary to previous claims based on genomic analyses.     

Repeated evolution and reversibility of self‐fertilization in the volvocine green algae*

Outcrossing and self‐fertilization are fundamental strategies of sexual reproduction, each with different evolutionary costs and benefits. Self‐fertilization is thought to be an evolutionary “dead‐end” strategy, beneficial in the short term but costly in the long term, resulting in self‐fertilizing species that occupy only the tips of phylogenetic trees. Here, we use volvocine green algae to investigate the evolution of self‐fertilization. We use ancestral‐state reconstructions to show that self‐fertilization has repeatedly evolved from outcrossing ancestors and that multiple reversals from selfing to outcrossing have occurred. We use three phylogenetic metrics to show that self‐fertilization is not restricted to the tips of the phylogenetic tree, a finding inconsistent with the view of self‐fertilization as a dead‐end strategy. We also find no evidence for higher extinction rates or lower speciation rates in selfing lineages. We find that self‐fertilizing species have significantly larger colonies than outcrossing species, suggesting the benefits of selfing may counteract the costs of increased size. We speculate that our macroevolutionary results on self‐fertilization (i.e., non‐tippy distribution, no decreased diversification rates) may be explained by the haploid‐dominant life cycle that occurs in volvocine algae, which may alter the costs and benefits of selfing.     

Evidence for speciational change in the evolution of ratites (Aves: Palaeognathae)

To perform a comparative analysis of character associations framed in a phylogenetic context (e.g. independent contrasts), a model of character evolution must be assumed. According to phyletic gradualism, morphological change accumulates gradually over time within lineages, and speciation events do not have a major role. Under speciational models, morphological change is assumed to occur during or just after cladogenesis in both daughter species, and the resulting morphologies do not change over long periods of time (stasis), until the next cladogenetic event. A novel method is presented for comparing these models of character evolution that uses permutational multiple phylogenetic regressions. The addition of divergence times to well-corroborated phylogenetic trees and the utilization of the method developed in this paper allows the estimation of relative frequency of gradual change and speciational change from living organisms. This method is applied to a dataset from ratites with the conclusion that, for a range of morphological features, change tends to have been speciational rather than gradual.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 80 , 99–106.     

Willi Hennig’s dichotomization of nature

Two formal assumptions implied in Willi Hennig’s “phylogenetic systematics” were repeatedly criticized for not being biologically grounded. The first is that speciation is always dichotomous; the second is that the stem‐species always goes extinct when its lineage splits into two daughter species. This paper traces the theoretical roots of Hennig’s “principle of dichotomy”. While often considered merely a methodological principle, Hennig’s realist perspective required him to ground the “principle of dichotomy” ontologically in speciation. As a methodological principle, the adherence to a strictly dichotomously structured phylogenetic system allowed Hennig to be unequivocal in character analysis and precise in the rendition of phylogenetic relationships. The ontological grounding of the “principle of dichotomy” in speciation remains controversial, however. This has implications for the application of techniques of phylogeny reconstruction to populations of bisexually reproducing organisms (phylogeography). Beyond that, the “principle of dichotomy” has triggered an intensive debate with respect to phylogeny reconstruction at the prokaryote level. © The Willi Hennig Society 2010.     

Claims and limits of phylogenetic systematics1

Within the methodology of phylogenetic systematics four hierarchic levels are distinguished: the “Central Claim” (to reconstruct phylogeny), methodoloical postulate (to conclude analysis with a purely dichotomous cladogram if ever possible), method (search for sister-group relationships by character analysis), and “Taxonomic Principle” (establishment of a classification reflecting merely the recognized genealoy). Certain limits of applicability and reliability of traditional phylogenetic systematics are specified: genealogy can only be analysed among taxa with perceptible evolutionary novelties; reticulated genealogy is not yet regarded; events other than cladogenetic ones cannot be recognised. Phylogenetic systematics is an independent method which has not been absorbed by any type of “pattern” or “transformed” cladism. Phylogenetic systematics relies on the theory of evolution, which does not lead into circularity, since phylogenetic systematics does not claim to prove or to explain evolution whatsoever.     

Evolution of interspecies unilateral incompatibility in the relatives of Arabidopsis thaliana

The evolutionary concurrence of intraspecies self‐incompatibility (SI) and explosive angiosperm radiation in the Cretaceous have led to the hypothesis that SI was one of the predominant drivers of rapid speciation in angiosperms. Interspecies unilateral incompatibility (UI) usually occurs when pollen from a self‐compatible (SC) species is rejected by the pistils of a SI species, while the reciprocal pollination is compatible (UC). Although this SI × SC type UI is most prevalent and viewed as a prezygotic isolation barrier to promote incipient speciation of angiosperms, comparative evidence to support such a role is lacking. We show that SI × SI type UI in SI species pairs is also common in the well‐characterized accessions representing the four major lineages of the Arabidopsis genus and is developmentally regulated. This allowed us to reveal a strong correlation between UI strength and species divergence in these representative accessions. In addition, analyses of a SC accession and the pseudo‐self‐compatible (psc) spontaneous mutant of Arabidopsis lyrata indicate that UI shares, at least, common pollen rejection pathway with SI. Furthermore, genetic and genomic analyses of SI × SI type UI in A. lyrata × A. arenosa species pair showed that two major‐effect quantitative trait loci are the stigma and pollen‐side determinant of UI, respectively, which could be involved in heterospecies pollen discrimination. By revealing a close link between UI and SI pathway, particularly between UI and species divergence in these representative accessions, our findings establish a connection between SI and speciation. Thus, the pre‐existence of SI system would have facilitated the evolution of UI and accordingly promote speciation.     

Evolutionary dynamics of mating system shifts in Arabidopsis lyrata

Outcrossing is the prevalent mode of reproduction in plants and animals despite its substantial costs, while selfing and mixed mating occur at much lower frequency. Comparative research on plants has demonstrated the lability of self‐incompatibility, but there is little information about the transition on a within‐species level from self‐incompatibility to predominant selfing. We studied variation in mating system among 18 populations of Arabidopsis lyrata within a phylogenetic context to shed light on the evolution of selfing. Realized and potential mating systems were assessed by genetic analysis with microsatellite markers and hand‐self‐pollinations on 30 plants from each population. The fraction of self‐incompatible plants in a population was highly correlated with the outcrossing rate, showing that the spread of self‐compatibility is accompanied by or soon followed by an increase in the rate of selfing. The four predominantly selfing populations (outcrossing rates < 0.25) fell into more than one phylogenetic cluster, suggesting that the transition to selfing occurred more than once independently. Hence, A. lyrata offers an opportunity for the comparative analysis of outcrossing as a predominant mode of reproduction in plants and of the causes of the shift to selfing.     

Conceptual and statistical problems with the DEC+J model of founder‐event speciation and its comparison with DEC via model selection

Phylogenetic studies of geographic range evolution are increasingly using statistical model selection methods to choose among variants of the dispersal‐extinction‐cladogenesis (DEC) model, especially between DEC and DEC+J, a variant that emphasizes “jump dispersal,” or founder‐event speciation, as a type of cladogenetic range inheritance scenario. Unfortunately, DEC+J is a poor model of founder‐event speciation, and statistical comparisons of its likelihood with DEC are inappropriate. DEC and DEC+J share a conceptual flaw: cladogenetic events of range inheritance at ancestral nodes, unlike anagenetic events of dispersal and local extinction along branches, are not modelled as being probabilistic with respect to time. Ignoring this probability factor artificially inflates the contribution of cladogenetic events to the likelihood, and leads to underestimates of anagenetic, time‐dependent range evolution. The flaw is exacerbated in DEC+J because not only is jump dispersal allowed, expanding the set of cladogenetic events, its probability relative to non‐jump events is assigned a free parameter, j, that when maximized precludes the possibility of non‐jump events at ancestral nodes. DEC+J thus parameterizes the mode of speciation, but like DEC, it does not parameterize the rate of speciation. This inconsistency has undesirable consequences, such as a greater tendency towards degenerate inferences in which the data are explained entirely by cladogenetic events (at which point branch lengths become irrelevant, with estimated anagenetic rates of 0). Inferences with DEC+J can in some cases depart dramatically from intuition, e.g. when highly unparsimonious numbers of jump dispersal events are required solely because j is maximized. Statistical comparison with DEC is inappropriate because a higher DEC+J likelihood does not reflect a more close approximation of the “true” model of range evolution, which surely must include time‐dependent processes; instead, it is simply due to more weight being allocated (via j) to jump dispersal events whose time‐dependent probabilities are ignored. In testing hypotheses about the geographic mode of speciation, jump dispersal can and should instead be modelled using existing frameworks for state‐dependent lineage diversification in continuous time, taking appropriate cautions against Type I errors associated with such methods. For simple inference of ancestral ranges on a fixed phylogeny, a DEC‐based model may be defensible if statistical model selection is not used to justify the choice, and it is understood that inferences about cladogenetic range inheritance lack any relation to time, normally a fundamental axis of evolutionary models.     

Genetic regulation of self‐incompatibility

Self‐incompatibility is a cell‐cell recognition system in higher plants that is based on the ability of the pistil to discriminate “self‐pollen from “non‐self"‐pollen. In the simplest systems, this recognition response is controlled by a single locus — the S‐locus — with multiple alleles. Pollination of a pistil with pollen bearing an S‐allele recognition factor identical to that expressed in the host plant stigma or style results in rejection of the “self"‐pollen. Most of the studies on the molecular genetics of self‐incompatibility that are summarized in this review have had as their goal the identification and characterization of the gene product(s) associated with the self‐incompatibility response. These studies have provided a great deal of new and important information about self‐incompatibility — despite the fact that many critical questions remain unresolved. Taken together, the present evidence from these studies indicates that the self‐incompatibility response is likely to be far more complex than suggested by historical models.     

Homomorphic Self‐Incompatibility,with Stylar Rejection Site,in Luehea grandiflora Mart. and Zucc. (Tiliaceae‐Malvaceae s.l.)

Abstract: The breeding system of Luehea grandiflora (Tiliaceae‐Malvaceae s.l.) was investigated using hand pollinations and fluorescence microscopy studies of pollen tube growth. Although selfed flowers persisted for some 10 days, our study indicates that L. grandiflora is self‐incompatible, with self pollen tube inhibition in the upper style, as occurs in many taxa with homomorphic, gametophytic self‐incompatibility (GSI). L. grandiflora is only the second species reported within the Malvales with homomorphic stylar inhibition. This result is discussed within the context of a report for self‐compatibility in this species, and we also consider the phylogenetic implications for the occurrence of GSI in the family Malvaceae s.l.     

INFLUENCE OF POLLINATION SPECIALIZATION AND BREEDING SYSTEM ON FLORAL INTEGRATION AND PHENOTYPIC VARIATION IN IPOMOEA

Natural selection should reduce phenotypic variation and increase integration of floral traits involved in placement of pollen grains on stigmas. In this study, we examine the role of pollinators and breeding system on the evolution of floral traits by comparing the patterns of floral phenotypic variances and covariances in 20 Ipomoea species that differ in their level of pollination specialization and pollinator dependence incorporating phylogenetic relatedness. Plants with specialized pollination (i.e., those pollinated by one functional group or by few morphospecies) displayed less phenotypic variation and greater floral integration than generalist plants. Self‐compatible species also displayed greater floral integration than self‐incompatible species. Floral traits involved in pollen placement and pick up showed less variation and greater integration than floral traits involved in pollinator attraction. Analytical models indicate that both breeding system and the number of morphospecies had significant effects on floral integration patterns although only differences in the former were significant after accounting for phylogeny. These results suggest that specialist/self‐compatible plants experience more consistent selection on floral traits than generalist/self‐incompatible plants. Furthermore, pollinators and breeding system promote integration of floral traits involved in pollen placement and pick up rather than integration of the whole flower.     

PHYLOGENETIC ANALYSIS OF TRAIT EVOLUTION AND SPECIES DIVERSITY VARIATION AMONG ANGIOSPERM FAMILIES

Angiosperm families differ greatly from one another in species richness (S). Previous studies have attributed significant components of this variation to the influence of pollination mode (biotic/abiotic) and growth form (herbaceous/woody) on speciation rate, but these results suffer difficulties of interpretation because all the studies ignored the phylogenetic relationships among families. We use a molecular phylogeny of the angiosperm families to reanalyse correlations between S and family-level traits and use reconstructions of trait evolution to interpret the results. We confirm that pollination mode and growth form are correlated with S and show that the majority of changes in pollination mode involved a change from biotic to abiotic pollination with an associated fall in speciation rate. The majority of growth form changes involved the evolution of herbaceousness from woodiness with a correlated rise in speciation rate. We test the hypothesis of Ricklefs and Renner (1994) that “evolutionary flexibility” rather than other trait changes triggered increased speciation rates in some families, but find little support for the hypothesis.     

Breeding systems in Balsaminaceae in relation to pollen/ovule ratio,pollination syndromes,life history and climate zone

• Pollen/ovule (P/O) ratios are often used as proxy for breeding systems. Here, we investigate the relations between breeding systems and P/O ratios, pollination syndromes, life history and climate zone in Balsaminaceae.
• We conducted controlled breeding system experiments (autonomous and active self‐pollination and outcrossing tests) for 65 Balsaminaceae species, analysed pollen grain and ovule numbers and evaluated the results in combination with data on pollination syndrome, life history and climate zone on a phylogenetic basis.
• Based on fruit set, we assigned three breeding systems: autogamy, self‐compatibility and self‐incompatibility. Self‐pollination led to lower fruit set than outcrossing. We neither found significant P/O differences between breeding systems nor between pollination syndromes. However, the numbers of pollen grains and ovules per flower were significantly lower in autogamous species, but pollen grain and ovule numbers did not differ between most pollination syndromes. Finally, we found no relation between breeding system and climate zone, but a relation between climate zone and life history.
• In Balsaminaceae reproductive traits can change under resource or pollinator limitation, leading to the evolution of autogamy, but are evolutionary rather constant and not under strong selection pressure by pollinator guild and geographic range changes. Colonisation of temperate regions, however, is correlated with transitions towards annual life history. Pollen/ovule‐ratios, commonly accepted as good indicators of breeding system, have a low predictive value in Balsaminaceae. In the absence of experimental data on breeding system, additional floral traits (overall pollen grain and ovule number, traits of floral morphology) may be used as proxies.

     

GENETIC DIFFERENTIATION,SYMPATRIC SPECIATION,AND THE ORIGIN OF A DIPLOID SPECIES OF STEPHANOMERIA

Evidence is presented that a geographically peripheral population of the annual Stephanomcria exigua ssp. coronaria (Compositae), a widespread and ecologically diverse species, has recently given rise by a process of sympatric speciation to a diploid species presently designated “Malheurensis.” The new species comprises less than 250 individuals and is found only at a single locality in eastern Oregon where it grows interspersed with its parental population. Stephanomeria exigua ssp. coronaria is an obligate outcrosser and “Malheurensis” is highly self-pollinating. Reproductive isolation is maintained by differences in breeding system, a crossability barrier that reduces seed set following cross-pollination between them, and reduction in hybrid fertility caused by chromosomal structural differences. They are very similar morphologically. Electrophoretic analyses of seven enzyme systems demonstrate that all the alleles but one at the controlling 13 gene loci in “Malheurensis” are identical to alleles in ssp. coronaria. The new species displays certain maladapted features including loss of the specific requirements for seed germination characteristic of the progenitor population of ssp. coronaria. The origin of “Malheurensis” appears to be an exception to the theory of geographical speciation because spatial isolation is not necessary at any time for the origin or establishment of its reproductive isolating barriers. The nature of these barriers plus the genetic homogeneity of the species are compatible with the hypothesis that it derives from a single progenitor individual. Very little genetic change is involved initially in this mode of speciation.     

Defining climate's role in ecosystem evolution: Clues from late quaternary mammals

Mammalian communities alter their taxonomic composition through time as the species composing them change their biogeographic range, become extinct, or evolve into new species. When taxonomic compositions change through these processes, inevitably the links between taxa and communities change too, resulting in evolution from one ecosystem into the next. Late Quaternary examples suggest that on a timescale encompassing a few thousand to a few hundred thousand years (the “multi‐millennial timescale"), climatic change is perhaps the most important driver of ecosystem evolution because it periodically forces biogeographic changes and extinction. Climatic change over this timescale, which essentially slips between “geological time”; and “ecological time”;, is not very closely in phase with population‐level evolution of a species analyzed for this study, the meadow vole Microtus pennsylvanicus; therefore climatic oscillations on the multi‐millennial timescale may not stimulate speciation much. Instead, speciation may contribute to ecosystem evolution independent of climatic change and over a longer time scale.     

Paraphyly,ancestors, and the goals of taxonomy: A botanical defense of cladism

Cronquist (1987) criticizes cladism for its rejection of paraphyletic groups, which he would retain if he feels they are “conceptually useful.” We argue that paraphyletic higher taxa are artificial classes created by taxonomists who wish to emphasize particular characters or phenetic “gaps,” and that formal recognition of such taxa conveys a misleading picture of common ancestry and character evolution. In our view, classifications should accurately reflect the nested hierarchy of monophyletic groups that is the natural outcome of the evolutionary process. Such systems facilitate the study of evolution and provide an efficient summary of character distributions. Paraphyletic groups, such as “prokaryotes,” “green algae,” “bryophytes,” and “gymnosperms,” should be abandoned, as continued recognition of such groups will only serve to retard progress in understanding evolution. Contrary to Cronquist’s (1987) assertions, cladistic theory is not at odds with standard views on speciation and the existence of ancestors. Groups of interbreeding organisms can continue to exist after giving rise to descendant species, and there are several ways in which such groups, whether extant or extinct, can be incorporated into cladistic classification. In contrast, paraphyletic higher taxa are neither cohesive (integrated by gene flow) nor whole, do not serve as ancestors, and are unacceptable in the phylogenetic system. Fossils may be of great value in assessing phylogenetic relationships and are readily accommodated in cladistic classification. Cladistic studies are helping to answer major questions about plant evolution, and we anticipate increased efforts to develop a truly phylogenetic system.     

THE EVOLUTION OF HYBRID INCOMPATIBILITIES ALONG A PHYLOGENY

The Dobzhansky–Muller model of speciation posits that defects in hybrids between species are the result of negative epistatic interactions between alleles that arose in independent genetic backgrounds. Tests of one important prediction from this model, that incompatibilities “snowball,” have relied on comparisons of the number of incompatibilities between closely related pairs of species separated by different divergence times. How incompatibilities accumulate along phylogenies, however, remains poorly understood. We extend the Dobzhansky–Muller model to multispecies clades to describe the mathematical relationship between tree topology and the number of shared incompatibilities among related pairs of species. We use these results to develop a statistical test that distinguishes between the snowball and alternative incompatibility accumulation models, including nonepistatic and multilocus incompatibility models, in a phylogenetic context. We further demonstrate that patterns of incompatibility sharing across species pairs can be used to estimate the relative frequencies of different types of incompatibilities, including derived–derived versus derived–ancestral incompatibilities. Our results and statistical methods should motivate comparative genetic mapping of hybrid incompatibilities to evaluate competing models of speciation.     

THE MICRO AND MACRO IN BODY SIZE EVOLUTION

The diversity of body sizes of organisms has traditionally been explained in terms of microevolutionary processes: natural selection owing to differential fitness of individual organisms, or to macroevolutionary processes: species selection owing to the differential proliferation of phylogenetic lineages. Data for terrestrial mammals and birds indicate that even on a logarithmic scale frequency distributions of body mass among species are significantly skewed towards larger sizes. We used simulation models to evaluate the extent to which macro- and microevolutionary processes are sufficient to explain these distributions. Simulations of a purely cladogenetic process with no bias in extinction or speciation rates for different body sizes did not produce skewed log body mass distributions. Simulations that included size-biased extinction rates, especially those that incorporated anagenetic size change within species between speciation and extinction events, regularly produced skewed distributions. We conclude that although cladogenetic processes probably play a significant role in body size evolution, there must also be a significant anagenetic component. The regular variation in the form of mammalian body size distributions among different-sized islands and continents suggests that environmental conditions, operating through both macro- and microevolutionary processes, determine to a large extent the diversification of body sizes within faunas. Macroevolution is not decoupled from microevolution.     

Breaking linkage between mating compatibility factors: Tetrapolarity in Microbotryum

Linkage of genes determining separate self‐incompatibility mechanisms is a general expectation of sexual eukaryotes that helps to resolve conflicts between reproductive assurance and recombination. However, in some organisms, multiple loci are required to be heterozygous in offspring while segregating independently in meiosis. This condition, termed “tetrapolarity” in basidiomycete fungi, originated in the ancestor to that phylum, and there have been multiple reports of subsequent transitions to “bipolarity” (i.e., linkage of separate mating factors). In the genus Microbotryum, we present the first report of the breaking of linkage between two haploid self‐incompatibility factors and derivation of a tetrapolar breeding system. This breaking of linkage is associated with major alteration of genome structure, with the compatibility factors residing on separate mating‐type chromosome pairs, reduced in size but retaining the structural dimorphism characteristic for regions of recombination suppression. The challenge to reproductive assurance from unlinked compatibility factors may be overcome by the automictic mating system in Microbotryum (i.e., mating among products of the same meiosis). As a curious outcome, this linkage transition and its effects upon outcrossing compatibility rates may reinforce automixis as a mating system. These observations contribute to understanding mating systems and linkage as fundamental principles of sexual life cycles, with potential impacts on conventional wisdom regarding mating‐type evolution.