Propagule pressure and the establishment of emergent polyploid populations.

BACKGROUND: Whereas the incidence or rate of polyploid speciation in flowering plants is modest, the production of polyploid individuals within local populations is widespread. Explanations for this disparity primarily have focused on properties or interactions of polyploids that limit their persistence. HYPOTHESIS: The emergence of local polyploid populations within diploid populations is similar to the arrival of invasive species at new, suitable sites, with the exception that polyploids suffer interference from their progenitor(s). The most consistent predictor of successful colonization by invasive plants is propagule pressure, i.e. the number of seeds introduced. Therefore, insufficient propagule pressure, i.e. the formation of polyploid seeds within diploid populations, ostensibly is a prime factor limiting the establishment of newly emergent polyploids within local populations. Increasing propagule number reduces the effects of genetic, environmental and demographic stochasticity, which thwart population survival. As with invasive species, insufficient seed production within polyploid populations limits seed export, and thus reduces the chance of polyploid expansion. CONCLUSION: The extent to which propagule pressure limits the establishment of local polyploid populations remains to be determined, because we know so little. The numbers of auto- or allopolyploid seed in diploid populations rarely have been ascertained, as have the numbers of newly emergent polyploid plants within diploid populations. Moreover, seed production by these polyploids has yet to be assessed.

Has the Polyploid Wave Ebbed?

There was a wave of whole genome duplications (WGD) during and subsequent to the K-Pg interface, which was followed by an increase in the proportion of species that were polyploid. I consider why this wave of polyploid speciation has continued to rise through the divergent evolution of polyploid lineages, and through rounds of homoploid and heteroploid chromosomal change. I also consider why the polyploid speciation wave is likely to rise in the next millennium. I propose that the speed of polyploid genesis through ploidal increase and through diversification among polyploids likely will be greater than the speed of diploid speciation. The increase in polyploid diversity is expected to lag well behind episodes of WGD, owing to the very long period required for species diversification either by lineage splitting or additional rounds of polyploidy, in addition to the long period of genomic adjustment to higher ploidal levels in neopolyploids.

Plant speciation in the age of climate change.

BACKGROUND: Species diversity is likely to undergo a sharp decline in the next century. Perhaps as many as 33 % of all plant species may expire as a result of climate change. All parts of the globe will be impacted, and all groups of organisms will be affected. Hundreds of species throughout the world have already experienced local extinction. PERSPECTIVES: While thousands of species may become extinct in the next century and beyond, species formation will still occur. I consider which modes of plant species formation are likely to prevail in the next 500 years. I argue that speciation primarily will involve mechanisms that produce reproductively isolated lineages within less (often much less) than 100 generations. I will not especially consider the human element in promoting species formation, because it will continue and because the conclusions presented here are unaffected by it. The impact of climate change may be much more severe and widespread. CONCLUSIONS: The most common modes of speciation likely to be operative in the next 500 years ostensibly will be auto- and allopolyploidy. Polyploid species or the antecedents thereof can arise within two generations. Moreover, polyploids often have broader ecological tolerances, and are likely to be more invasive than are their diploid relatives. Polyploid species may themselves spawn additional higher level polyploids either through crosses with diploid species or between pre-existing polyploids. The percentage of polyploid species is likely to exceed 50 % within the next 500 years vs. 35 % today. The stabilized hybrid derivatives (homoploid hybrid speciation) could emerge within a hundred generations after species contact, as could speciation involving chromosomal rearrangements (and perhaps number), but the number of such events is likely to be low. Speciation involving lineage splitting will be infrequent because the formation of substantive pre- and post-zygotic barriers typically takes many thousands of years.

Factors promoting polyploid persistence and diversification and limiting diploid speciation during the K-Pg interlude.

The large wave of polyploidization following the Cretaceous-Paleogene (K-Pg) mass extinction has been explained by enhanced polyploid persistence arising from adaptive properties of the polyploids themselves, as well as an increase in unreduced gamete production and diploid hybridization. We propose that the demise of diploids afforded opportunities for polyploid establishment and expansion into novel habitats. Augmented polyploid gene pools from diploid and polyploid relatives, in association with their multiple and independent origins (of both autopolyploids and allopolyploids), facilitated their subsequent diversification. Their ability to recruit genetic variation from their diploid relatives or from products of recurrent origins sharing their genome(s) ostensibly contributed to polyploid persistence. Concomitantly, we propose that the number of congeneric diploid species dramatically contracted disproportionally to polyploids during the K-Pg interval (i.e. a diploid trough), resulting in a reduction in the rate of diploid speciation. Accordingly, the preponderance of neopolyploids was likely autopolyploids.

On the young age of intraspecific herbaceous taxa.

Dated phylogenies rarely include the divergence times of sister intraspecific taxa, and when they do little is said about this subject. We show that over 90% of the intraspecific plant taxa found in a literature search are estimated to be 5 million yr old or younger, with only 4% of taxa estimated to be over 10 million yr old or older. A Bayesian analysis of intraspecific taxon ages indicates that indeed these taxa are expected to be < 10 million yr old. This result for the young age of intraspecific taxa is consistent with the earlier observation that post-pollination reproductive barriers develop between 5 and 10 million yr after lineage splitting, thus leading to species formation. If lineages have not graduated to the species level of divergence by 10 million yr or so, they are likely to have gone extinct by that time as a result of narrow geographical distributions, narrow niche breadths, and relatively small numbers across populations.

Critical factors in the establishment of allopolyploids.

PREMISE OF THE STUDY: The growth and spread of new polyploid populations have been explained in terms of fitness advantages over their diploid progenitors. However, a fitness advantage is not sufficient to insure the establishment of a polyploid; it must also overcome the obstacles of demographic stochasticity and minority disadvantage. Several studies have addressed the population dynamics of autopolyploids, but the present study is the first to consider allopolyploids, which are affected by more factors than autopolyploids. METHODS: We constructed a population dynamic model of four types of plants (two parent species, hybrids, allopolyploids) that also included an explicit breeding system. KEY RESULTS: The numbers of plants of each type were the most important factors determining whether the new allopolyploid would become established. More polyploid plants greatly increased the likelihood of polyploid persistence. More plants of the parent species and more hybrids resulted in more polyploids being produced. The model parameters with the most effect on polyploid establishment were potential population size (K), individual plant fecundity, and niche separation (α). The most important breeding system parameters were selfing rates, which mitigated minority disadvantage imposed by pollen limitation. CONCLUSIONS: The importance of population sizes, and the parameters that controlled them, in overcoming demographic stochasticity parallels the well-recognized role of propagule pressure in determining the success of invasive species. We modeled the establishment of a new allopolyploid; analogous considerations would affect the establishment of a new autopolyploid. The critical role of population sizes in polyploid establishment should be more widely recognized.

Polyploid formation shapes flowering plant diversity.

Polyploidy, or whole genome duplication, has been an important feature of eukaryotic evolution. This is especially true in flowering plants, where all extant angiosperms have descended from polyploid species. Here we present a broad comparative analysis of the effect of polyploidy on flowering plant diversity. We examine the widely held hypothesis that polyploid flowering plants generate more diversity than their diploid counterparts, by fitting stochastic birth/death models to observed ploidal frequency data from 60 extant angiosperm genera. Our results suggest the opposite, that diploids speciate at higher rates than polyploids, through a combination of simple diploid speciation and tetraploidy. Importantly, the estimated diploid advantage stemmed primarily from a higher rate of polyploidization in diploids than polyploids. Our model is also able to account for the empirically observed correlation between polyploidy and species richness without assuming that polyploids have a speciation advantage over diploids.

The timetable for allopolyploidy in flowering plants.

BACKGROUND: Our understanding of the processes and dynamics of allopolyploid speciation, the long-term consequences of ploidal change, and the genetic and chromosomal changes in new emerged allopolyploids has substantially increased during the past few decades. Yet we remain uncertain about the time since lineage divergence when two taxa are capable of spawning such entities. Indeed, the matter has seemed intractable. Knowledge of the window of opportunity for allopolyploid production is very important because it provides temporal insight into a key evolutionary process, and a temporal reference against which other modes of speciation may be measured. SCOPE: This Viewpoint paper reviews and integrates published information on the crossability of herbaceous species and the fertility of their hybrids in relation to species' divergence times. Despite limitations in methodology and sampling, the estimated times to hybrid sterility are somewhat congruent across disparate lineages. Whereas the waiting time for hybrid sterility is roughly 4-5 million years, the waiting time for cross-incompatibility is roughly 8-10 million years, sometimes considerably more. Strict allopolyploids may be formed in the intervening time window. The progenitors of several allopolyploids diverged between 4 and 6 million years before allopolyploid synthesis, as expected. This is the first study to propose a general temporal framework for strict allopolyploidy. This Viewpoint paper hopefully will stimulate interest in studying the tempo of speciation and the tempo of reproductive isolation in general.

Molecular signatures of selection on reproductive character displacement of flower color in Phlox drummondii.

Character displacement, which arises when species diverge in sympatry to decrease competition for resources or reproductive interference, has been observed in a wide variety of plants and animals. A classic example of reproductive character displacement, presumed to be caused by reinforcing selection, is flower-color variation in the native Texas wildflower Phlox drummondii. Here, we use population genetic analyses to investigate molecular signatures of selection on flower-color variation in this species. First, we quantify patterns of neutral genetic variation across the range of P. drummondii to demonstrate that restricted gene flow and genetic drift cannot explain the pattern of flower-color divergence in this species. There is evidence of extensive gene flow across populations with different flower colors, suggesting selection caused flower-color divergence. Second, analysis of sequence variation in the genes underlying this divergence reveals a signature of a selective sweep in one of the two genes, further indicating selection is responsible for divergence in sympatry. The lack of a signature of selection at the second locus does not necessarily indicate a lack of selection on this locus but instead brings attention to the uncertainty in depending on molecular signatures to identify selection.

Mating system shifts on the trailing edge.

BACKGROUND: The trailing edges of species ranges are becoming a subject of increasing interest as the environment changes due to global warming. Trailing edge populations are likely to face extinction because of a decline in numbers and an inability to evolve new adaptations with sufficient speed. Discussions of character change in the trailing edge have focused on physiological, exomorphic and phenological traits. The mating pattern within populations has not been part of the discourse, in spite of the fact that the mating pattern may affect the ability of populations to respond to environmental change and to maintain their sizes. In this paper, the case is made that a substantial increase in self-fertilization rates may occur via plastic responses to stress. SCOPE AND CONCLUSIONS: Small populations on the trailing edge are especially vulnerable to environmental change because of inadequate levels of cross-fertilization. Evidence is presented that a deficiency of cross-seed production is due to inadequate pollinator services and a paucity of self-incompatibility alleles within populations. Evidence also is presented that if plants are self-compatible, self-fertilization may compensate in part for this deficiency through a stress-induced increase in levels of self-compatibility and stress-induced alterations in floral morphology that elevate self-pollination. Whereas increased self-fertility may afford populations the time to adapt to their changing environments, it can be concluded that increased selfing is not a panacea for the ills of environmental change, because it will lead to substantial reductions in genetic diversity, which may render adaptation unlikely.

Social dilemmas among supergenes: intragenomic sexual conflict and a selfing solution in Oenothera.

Recombination is a powerful policing mechanism to control intragenomic cheats. The "parliament of the genes" can often rapidly block driving genes from cheating during meiosis. But what if the genome parliament is reduced to only two members, or supergenes? Using a series of simple game-theoretic models inspired by the peculiar genetics of Oenothera sp., we illustrate that a two supergene genome (α and ß) can produce a number of surprising evolutionary dynamics, including increases in lineage longevity following a transition from sexuality (outcrossing) to asexuality (clonal self-fertilization). We end by interpreting the model in the broader context of the evolution of mutualism, which highlights that greater α, ß cooperation in the self-fertilizing model can be viewed as an example of partner fidelity driving multilineage cooperation.

Flowering-time plasticity facilitates niche shifts in adjacent populations.

The potential for a habitat shift is enhanced when selection against immigrants is augmented by a temporal difference between them and inhabitants of core populations. Genetically mediated changes in flowering time often accompany niche shifts in plants. The possibility that temporal change may arise from plastic responses to novel, stressful, environments rather than from genetic alteration has not been explored. This option is considered here, and it may be quite common. The substantial literature on transplant and common garden experiments shows that invaders of novel habitats are likely to undergo a developmentally based phenological shift. A phenological change in the invading population leads to assortative mating within populations, which in turn facilitates the evolution of local adaptation by the invader. Environmental induction may be the sole contributor to temporal change, or this factor may act in concert with genetic change. Flowering shifts based on developmental responses are immediate, not subject to remediation by gene flow and not affected by a paucity of genetic variation, negative genetic correlations or antagonistic pleiotropy, all of which might constrain phenological evolution.

On the abundance of polyploids in flowering plants.

The wide distribution of polyploidy among plants has led to a variety of theories for the evolutionary advantages of polyploidy. Here we claim that the abundance of polyploidy may be the result of a simple ratcheting process that does not require evolutionary advantages due to the biological properties of organisms. The evolution of polyploidy is a one-way process in which chromosome number can increase but not decrease. Using a simple mathematical model, we show that average ploidal level within a plant lineage can continually increase to the levels observed today, even if there are ecological or physiological disadvantages to higher ploidy. The model allowed us to estimate the average net speciation and polyploidy rates for ten angiosperm genera. Based on these estimates, the model predicts distributions of ploidal levels statistically similar to those observed in nine of the 10 genera.

Phyletic hot spots for B chromosomes in angiosperms.

We determined whether supernumerary B chromosomes were nonrandomly distributed among major angiosperm lineages and among lineages within families, as well as the identity of lineages with unusually high B-chromosome frequencies (hot spots). The incidence of B chromosomes for each taxon was gathered from databases showing species with and without these chromosomes (among species with known chromosome numbers). Heterogeneity was found at all ranks above the species level. About 8% of monocots had B chromosomes versus 3% for eudicots; they were rare in nonmonocot basal angiosperms. Significant heterogeneity in B-chromosome frequency occurred among related orders, families within orders, and major taxa within families. There were many B-chromosome hot spots, including Liliales and Commelinales at the order level. At the family level, there was a trend suggesting that B-chromosome frequencies are positively correlated with genome size.

A model for chloroplast capture.

Chloroplast capture, the introgression of a chloroplast from one species into another, has been frequently suggested as the explanation for inconsistencies between gene trees based on nuclear and cytoplasmic markers in plants. We use a genetic model to determine the conditions for capture to occur, and we find that they are somewhat more general than those given in earlier verbal arguments. Chloroplast capture can occur if cytoplasm substitution provides an advantage in seed production. This can happen through reallocation to the female function when cytonuclear incompatibilities cause partial male sterility, but also under more general conditions. Capture is promoted by nuclear incompatibilities between the two genomes (or a low heterosis in F1 hybrids) and by partial selfing when hybridization causes a decrease in the selfing rate and inbreeding depression is strong. We discuss empirical predictions that can be used to test this mechanism.

RESPONSE TO SELECTION ON AUTOGAMY IN PHLOX.

Two cycles of artificial selection were performed to increase autogamous fruiting in two wild populations of the self-incompatible Phlox drummondii, to decrease autogamous fruiting in two wild populations of the self-compatible Phlox cuspidata, and to both increase and decrease autogamous fruiting in a cultivar of P. drummondii which is pseudo-self-compatible. The breeding systems were determined to be genetically quite flexible, independent of inbreeding depression and other genetic phenomena which could hinder a breeding system shift. This is especially true for increasing autogamy. Self-pollen-pistil compatibility seems to be the single character affected by selection. Based on the continuous variation in both autogamy and self-compatibility, we suggest that the change has been due to genes which modify the self-incompatibility reaction rather than to the simple segregation of alleles at the S-locus.