Whole-genome duplication (polyploidy) is among the most frequent routes to reproductive isolation in plants, yet Mayrose, Zhan, Rothfels, Magnuson-Ford, Barker, Rieseberg and Otto (Science, 2011) showed that recently formed polyploid lineages diversify at lower rates than their diploid relatives, implying elevated extinction among neopolyploids. The paper explicitly left open whether the polyploid lineages that survive this early filter go on to attain greater long-term evolutionary success — for example, higher net diversification over deep time — as a consequence of their expanded genomic potential, and it noted as a limitation of its own analysis that its estimates of the frequency of heteroploid speciation likely represent upper bounds, because only phylogenies with variation in ploidy were examined and ploidy transitions were allowed only at speciation events. The subsequent literature shows that the long-term-success question remains genuinely open: post-2011 comparative studies across angiosperm clades yield clashing, clade-specific answers; the mechanistic literature on neopolyploid establishment is theoretical or case-level; and although joint anagenetic–cladogenetic models of ploidy change have since been substantially developed, a general verdict on the long-term success of polyploid survivors is still missing, and empirical macroevolutionary diploidization rates (the transition of polyploid genomes back to diploid-like gene content and chromosome numbers) remain unquantified.

Background

Polyploidy (whole-genome duplication, WGD) is the condition of possessing more than two complete sets of chromosomes; it arises either by genome doubling within a lineage (autopolyploidy) or by hybridization between species whose genomes double to restore pairing (allopolyploidy). A newly formed polyploid individual or population is a neopolyploid. Because polyploids are reproductively isolated from their diploid progenitors essentially at formation, polyploidization is a mode of speciation; a speciation event that involves a change in ploidy is called heteroploid speciation. In phylogenetic comparative biology, the net diversification rate of a lineage is its speciation rate minus its extinction rate, and a lineage is evolutionarily 'successful' on the macroevolutionary scale if its net diversification exceeds that of comparable diploid lineages over deep time. Over evolutionary time, polyploid genomes tend to undergo diploidization — genome restructuring, gene loss, and dysploid (stepwise, non-doubling) chromosome-number change that gradually returns polyploid genomes toward diploid-like gene content and chromosome numbers — so long-term persistence and diploidization dynamics are linked. State-specification-and-extinction (SSE) models are likelihood-based phylogenetic frameworks that jointly estimate character-state transitions (here, ploidy changes) and state-dependent speciation/extinction rates from a dated phylogeny with observed tip states; chromosome-number evolution models such as chromEvol treat ploidy change either along branches (anagenetic) or at speciation events (cladogenetic). The quantitative backdrop: Otto and Whitton (Annual Review of Genetics, 2000) estimated that roughly 2–4% of speciation events in flowering plants and about 7% in ferns involved a ploidy increase, while noting that conclusive evidence for an effect of polyploidy on diversification rates was lacking. Wood, Takebayashi, Barker, Mayrose, Greenspoon and Rieseberg (PNAS, 2009) estimated that about 15% of angiosperm and 31% of fern speciation events were polyploid, and that about 35% of vascular-plant species (34.5% of the 28,406 species they surveyed across vascular-plant genera) are recent polyploids — yet also found no direct evidence that established polyploid lineages enjoy higher net diversification. Mayrose et al. (Science, 2011) then fitted ploidy-dependent diversification models (BiSSE-type models — binary state speciation and extinction models, likelihood frameworks that estimate speciation and extinction rates separately for two character states, here diploid versus polyploid — and related hidden-state extensions) to a diverse set of dated vascular-plant phylogenies with inferred tip ploidy, together encompassing hundreds of inferred polyploidization events, and found that polyploids, especially neopolyploids, have on average higher extinction and lower net diversification rates than diploids — so that, paradoxically, the most frequent mode of plant speciation appears on average to be an evolutionary dead end. Their analyses operated on generic-level phylogenies, defining neopolyploids as lineages that underwent polyploidization since divergence from their generic ancestor; they fixed the polyploid-to-diploid transition rate at zero in the main analyses and defended that constraint in the supporting material, where they argued that polyploid-to-diploid reversions are virtually unknown in the plant world and that only under unrealistically high reversion rates would polyploids be likely to diversify at rates as high as that inferred for diploids. They acknowledged one limitation of their frequency estimates: their estimates of the rate at which diploids speciate via polyploidization likely represent upper bounds, because only phylogenies with variation in ploidy were examined and because ploidy transitions were allowed only at speciation events. The open question they explicitly left — the problem stated here — is whether the polyploid lineages that persist past this early extinction filter go on to attain greater long-term evolutionary success (for example, elevated diversification over deep macroevolutionary timescales) because of their expanded genomic potential (duplicated genes free to diverge, larger buffering capacity, ecological tolerance).

Problem Statement

Determine the macroevolutionary fate of polyploid plant lineages, as left open by Mayrose et al. (2011). The common scientific objective is to establish, with quantitative phylogenetic and mechanistic evidence, whether polyploidy — after its well-documented short-term cost — is a net engine of long-term plant diversification, and why. Specifically, test whether polyploid lineages that survive the initial extinction bottleneck attain greater long-term evolutionary success, in the sense of elevated net diversification over deep (macroevolutionary) time relative to comparable diploid lineages, and whether any such elevation is attributable to their expanded genomic potential. Because the source's short-term result was established on generic-level phylogenies, with neopolyploids defined relative to the generic ancestor, extending the comparison to deeper macroevolutionary time is itself part of the empirical question, including how the polyploid lineages that persist past the early filter and the appropriate diploid comparison lineages are to be identified on dated phylogenies. Related quantities inform the interpretation of any verdict but are not separately required to resolve it: the mechanisms responsible for the elevated extinction of newly formed polyploids; the rates and temporal dynamics of diploidization — the transition of polyploid lineages toward diploid-like gene content and chromosome behavior — and how these rates influence long-term persistence; and corrected estimates of the contribution of polyploid formation to plant diversification, for which the source's own heteroploid-speciation frequencies are an acknowledged upper bound. The open question left by the source, however, is the long-term success of persisting polyploids itself.

References

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