Plant Speciation
Abstract
Like the formation of animal species, plant speciation is characterized by the evolution of barriers to genetic exchange between previously interbreeding populations. Prezygotic barriers, which impede mating or fertilization between species, typically contribute more to total reproductive isolation in plants than do postzygotic barriers, in which hybrid offspring are selected against. Adaptive divergence in response to ecological factors such as pollinators and habitat commonly drives the evolution of prezygotic barriers, but the evolutionary forces responsible for the development of intrinsic postzygotic barriers are virtually unknown and frequently result in polymorphism of incompatibility factors within species. Polyploid speciation, in which the entire genome is duplicated, is particularly frequent in plants, perhaps because polyploid plants often exhibit ecological differentiation, local dispersal, high fecundity, perennial life history, and self-fertilization or asexual reproduction. Finally, species richness in plants is correlated with many biological and geohistorical factors, most of which increase ecological opportunities.
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We thank the great botanical naturalists of the 20th century who provided the foundation for current studies of plant speciation. These include the founding fathers of ecological genetics (J. Clausen, D. Keck, and W. Hiesey), the grand synthesizers (G. L. Stebbins and Verne Grant), and the hybridization enthusiast, Edgar Anderson. We also thank members of the Rieseberg and Willis laboratories and three referees for useful comments on an earlier version of this paper. The authors' research on speciation has been supported by NSF, NIH, USDA, and the National Sciences and Engineering Research Council of Canada.
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Volume 317 | Issue 5840
17 August 2007
17 August 2007
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American Association for the Advancement of Science.
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Published in print: 17 August 2007
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RE: the response of Riesberg (2007) to Forsdyke's eLetter
For a further amplification of Forsdyke's viewpoint, please see:
Forsdyke, D. R. (2010) Notes and Records of the Royal Society 64, 139-154 (doi:10.1098/rsnr.2009.0045) George Romanes, William Bateson, and Darwin's "Weak Point."
Forsdyke, D.R (2016) Evolutionary Bioinformatics. 3rd Edition. Springer, New York.
Response to D. R. Forsdyke's E-Letter
It is true that Bateson ultimately concluded that he didn't know how species formed and that Darwinism in general, and genetics in particular, had failed to find a solution to the species problem (1). This is discussed in detail in Orr's (2) original article on Bateson (p. 1334). However, despite these later doubts, Bateson's 1909 model for the evolution of hybrid sterility (3) is essentially identical to that later put forward by Dobzhansky (4) and Muller (5). Indeed, Bateson [(3), quoted in (2)] writes, "when two species, both perfectly fertile severally, produce on crossing a sterile progeny, there is a presumption that the sterility is due to the development in the hybrid of some substance which can be formed only by meeting of two complementary factors."
Thus, while BDM may be an example of a runaway meme, recognizing Bateson for his early recognition of how hybrid incompatibilities evolve is long overdue.
Loren H. Rieseberg
Department of Botany, University of British Columbia, Vancouver BC V6T 1Z4, Canada.
John H. Willis
Department of Biology, Duke University, Durham, NC 27708, USA.
References
1. W. Bateson, Science 55, 55 (1922).
2. H. A. Orr, Genetics 144, 1331 (1996).
3. W. Bateson, in Darwin and Modern Science, A.C. Seward, Ed. (Cambridge University Press, Cambridge, 1909).
4. T. Dobzhansky, Genetics and the Origin of Species (Columbia University Press, New York, 1937).
5. H. J. Muller, Biol. Symp. 6, 71 (1942).
A False Batesonian Meme
In their Review of plant speciation (17 August 2007, p. 910), L. H. Rieseberg and J. H. Willis refer to the Bateson-Dobzhansky-Muller (BDM) model for the process by which incompatibilities between genes can lead to divergence between members of a species such that two new species emerge (1). It would be difficult to find a more prestigious trio to back a model than William Bateson, Theodosius Dobzhansky and Herman J. Muller. It was Bateson who brought Mendel to the attention of the English-speaking world and in 1905 suggested "genetics" as the name for the new discipline.
However, from 1902 onwards, Bateson, in paper after paper, declared that it was most unlikely that the Mendelian character units, which were transferable by cross-breeding and became known as genes, were involved in the initiation of speciation. Much of this was summarised in 1922 in his Toronto address to the American Association for the Advancement of Science (2): "[Genetic] analysis has revealed hosts of transferable characters [genes]. Their combinations suffice to supply an abundance of [pheno]types which might pass for new species, and certainly would be so classed if they were met with in nature. Yet critically tested [by crossing], we find that they are not distinct species and we have not reason to suppose that any accumulation of characters of the same order [transferable characters amenable to conventional genetic analysis] would cumulate in the production of distinct species. ... Specific difference [that which is responsible for speciation] therefore must be regarded as probably attached to the base upon which these transferables are implanted, of which we know absolutely nothing at all."
Up to his death in 1926, Bateson remained strongly opposed to genic models, because he thought that something beyond genes (the base) was involved. His dilemma was whether that something was located chromosomally with the genes, or was elsewhere. Today, the something can be seen as the base composition (GC%) accent of DNA (3–5).
In their first formulations of the DM model in the 1930s, neither Dobzhanshy nor Muller cited Bateson, probably because they knew his views were diametrically opposed to their own (6, 7). Nevertheless, in 1996 a member of the genic school claimed that Bateson had antecedently derived the Dobzhansky-Muller hypothesis (8). The error was soon reiterated (9, 10), and in 2000 first became dignified with the acronym "BDM" (11). Gathering momentum, in 2001 BDM began to appear in textbooks and reviews (12–15). Soon it had spread to Science (16), Nature Genetics(17), and Nature (18). With the Reiseberg-Willis paper it returns again to Science.
My attempts to stem the flood of misinformation (3–5) seem to have been to no avail, and I fear that my newest attempt (19) will be similarly unproductive. It seems that we have here another example of a runaway "meme" (20).
Donald R. Forsdyke
Department of Biochemistry, Queen's University, Kingston, ON K7L3N6, Canada.
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8. H. A. Orr, Genetics 144, 1331 (1996).
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