Why Is Speciation By Polyploidy More Likely In Plants Than In Animals?

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Plant Speciation

Loren H. Rieseberg

ⁱ Department of Botany, University of British Columbia, Vancouver, BC V6T 1Z4, Canada

² Department of Biology, Indiana Academy, Bloomington, IN 47405, USA

John H. Willis

³ Department of Biology, Duke University, Durham, NC 27708, U.s.

Abstruse

Like the formation of beast 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 than to full reproductive isolation in plants than practice 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 oftentimes result in polymorphism of incompatibility factors within species. Polyploid speciation, in which the entire genome is duplicated, is peculiarly frequent in plants, perhaps considering polyploid plants often exhibit ecological differentiation, local dispersal, loftier 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.

Plants provide extraordinary opportunities for studying speciation. Flowering plants are specially speciose, abaft merely insects in named species diversity. Much of this diversification has occurred recently, creating spectacular examples of adaptive radiations and of speciation in action (table S1). Plants are by and large sessile but vary dramatically in mating system, ploidy level, mode of dispersal, and life history, aiding efforts to sympathize the contribution of diverse ecological and evolutionary factors to speciation.

What Is a Institute Species?

The definition of a species in plants has been a major impediment to botanical studies of speciation; botanists have oftentimes expressed incertitude that establish species even exist, considering of frequent reports of interspecific hybrids (one) and because phenotypic variation in some plant groups does non assort readily into discrete categories (2). These concerns were amplified past claims that factor menstruum inside many establish species was so low that populations rather than species were the almost inclusive reproductive units (2, iii).

Recent work allays these concerns. Analyses of morphometric information from more than than 200 plant genera point that discrete clusters of morphologically like individuals occur inside nearly sexual plant lineages, that these clusters stand for closely to groups with significant mail service-pollination reproductive isolation, and that interspecific hybridization is non the master cause of poorly defined species boundaries (4). Molecular population genetic studies imply that migration rates within plant species are higher than before direct estimates and practice non differ, on boilerplate, from those of animals (5). Theoretical (6) and empirical work further indicates that even in species with low cistron menstruation, populations may evolve in concert through the spread of advantageous alleles (vii).

Although many plant species are held together by gene menstruum and kept apart from other species by reproductive barriers, there are exceptions. For example, some plants reproduce without sexual activity. These asexual taxa are composed of clonal hybrid genotypes that fill up the phenotypic infinite between their sexual parental species (table S1). Considering sexual reproduction is infrequent in such species, information technology is difficult to hash out their evolution in terms of sexual isolation and speciation. In dissimilarity, self-fertilizing (selfing) species oft maintain genetic and phenotypic cohesion (4) considering they have higher inside-species gene menstruum than previously hypothesized (viii), and their restricted outcrossing (exchange of pollen betwixt individuals) impedes interspecific hybridization. Reproductive isolation betwixt species may be incomplete, however, particularly in groups that have recently undergone multiple speciation events or those that have long generation times. This incomplete isolation may consequence in some gene menstruation between groups that are otherwise well-defined species (tabular array S1).

Reproductive Isolation

Reproductive isolation is non the proximal cause of diversification; this is the province of diversifying option and genetic drift. However, reproductive isolation tin facilitate the aggregating of genetic differences betwixt groups of populations, thereby sharpening boundaries betwixt them and permitting adaptive traits to motion closer to their fettle optima. This does non require absolute isolation. Rather, any reduction in the effective migration rate facilitates divergence, which reduces effective migration rates even farther. The resulting feedback loop, given enough time, usually leads to consummate genetic isolation.

Multiple reproductive barriers isolate nearly plant species. These include prepollination barriers that limit the transfer of pollen from individuals of i species to stigmas of other species. Several prepollination barriers—ecogeographic, mechanical, and temporal—are establish in animal species, whereas pollinator isolation is exclusively associated with constitute speciation. Other barriers, such as an advantage of conspecific pollen in fertilizing eggs compared with nonconspecific pollen (conspecific pollen precedence) and the failure of nonconspecific pollen to fertilize eggs (gametic incompatibilities), act after pollination only before fertilization, resulting in postpollination, prezygotic isolation. A final set of barriers, too establish in animals, act after fertilization: hybrid inviability, sterility, and the failure or reduction in successful reproduction in subsequent generations (hybrid breakdown). These postzygotic barriers may be a past-product of changes in the internal genetic environment (intrinsic isolation) or in the external ecological environs (extrinsic isolation). Current challenges are to gauge the relative contribution of unlike reproductive barriers in limiting cistron menstruum amid contemporary populations and to determine the guild and speed with which they arose.

All else beingness equal, early on-acting reproductive barriers volition contribute more to isolation than late-acting barriers (nine). For instance, the production of hybrid seeds in artificial crosses and reductions in the fertility of start-generation hybrids are commonly tested in the greenhouse. Cross-compatibility information (4) reveals that hybrid fertility reduction is the slightly stronger of the two barriers. Still, because hybrid seed production acts earlier reductions in fertility, reduced hybrid seed production really would exist expected to contribute almost 75% and hybrid sterility simply 25% of the total isolation caused by these two barriers.

Unfortunately, only a few studies provide comprehensive estimates of isolation between pairs of sibling species (table S1). In these, the cumulative effects of many reproductive barriers lead to almost complete isolation. Early-acting reproductive barriers such equally ecogeographic, pollinator, and mating system isolation are nearly important (table S1 and fig. S1), whereas tardily-interim postzygotic barriers contribute very piffling to isolation. Ecogeographic isolation has long been viewed every bit the well-nigh of import reproductive bulwark in plants (10), and its preeminence has been confirmed past numerous reciprocal transplant studies showing differences in habitat preferences amongst closely related species or subspecies (Tabular array 1). Pollinator and mating system isolation are less frequent, with the former arising when the focal species is numerically ascendant but does not fully apply the array of available animal pollinators (11).

Table 1

Case studies of plant speciation.

Topic	Taxa studied	Conclusions	Ref.
Reproductive isolation	Gilia capitata ssp. capitata and G. c. ssp. chamissonis	Local adaptation of interfertile subspecies to different habitats restricts successful migration and factor period.	(48)
	Chill Draba	Three self-fertilizing morphological species each appears to comprise thousands of cryptic biological species.	(49)
Genetics of isolation	Mimulus lewisii and Chiliad. cardinalis	Allele increasing petal carotenoid concentration reduced bee visitation by fourscore%; allele increasing nectar production doubled hummingbird visitation.	(50)
	Lycopersicon hirsutum and L. pimpinellifolium	Tomato lines with resistance cistron (Cf-two) from Fifty. pimpinellifolium showroom autonecrosis of mature leaves, but no autonecrosis observed when complementary gene (RC3) from S. pimpinellifolium as well introduced.	(51)
Hybrid and polyploid speciation	Helianthus anomalus, H. deserticola, and H. paradoxus	Three diploid species arisen via hybridization from same ii parental species. Karyotypically divergent hybrids colonized farthermost habitats through selection on transgressive traits (Fig. ii).	(52)
	Brassica napus	Chromosomal rearrangement after polyploidization responsible for flowering time departure among synthetic polyploid lineages.	(53)
Factors affecting species richness	Angiosperms	Conquering of nectar spurs in wide multifariousness of plants correlated with increased species multifariousness.	(44)
	Andean Lupinus	Nigh rapid species radiation in plants driven by ecological opportunities afforded past uplift of Andes.	(54)

It is difficult to decide the order of reproductive barrier evolution. Indirect bear witness from analyses of patterns of reproductive isolation suggests that prepollination barriers often arise first. For example, 19% of 1234 interspecific cantankerous combinations (virtually from rapidly radiating lineages isolated by ecological barriers) failed to prove evidence of cantankerous-incompatibility or intrinsic postzygotic isolation (4). Intrinsic postzyotic barriers may arise first in polyploid species that are intersterile with their diploid progenitors only that fail to exhibit ecological differences (tabular array S1). Likewise, intrinsic post-zygotic barriers may sometimes arise before ecological barriers (other than mating system isolation) in selfing species (Tabular array 1).

We know surprisingly trivial nearly the speed of plant speciation, although studies of gimmicky evolution imply that reproductive barriers tin arise speedily. For instance, grass populations exposed to different fertilizer treatments or to mine tailings exhibit both temporal (flowering time) and habitat isolation (seeds transplanted between sites have reduced survival) (tabular array S1). Interestingly, flowering time divergence is greatest at the boundary betwixt habitats in both experiments, a design suggestive of reinforcement, where selection against unfit hybrids has enhanced prezygotic isolation. These studies of speciation in action illustrate the plausibility of reinforcement and sympatric speciation, both of which are increasingly well supported by theory (12) and empirical work (table S1).

Although individual reproductive barriers can arise rapidly, most establish species remain separated past numerous barriers, which implies that complete speciation typically requires many thousands of generations. The main exceptions to this are hybrid and polyploid speciation. Fully isolated polyploid species may arise in i or 2 generations, and diploid or homoploid hybrid species may achieve isolation in as few as sixty generations (xiii).

Genetics of Isolation

Genetic analyses provide information on the numbers and kinds of genetic changes underlying reproductive barriers, equally well as on the evolutionary forces responsible for their origin. Studies of pollinator isolation have shown, for example, that major quantitative trait loci (QTLs) sometimes underlie shifts in the animals that pollinate plants (pollination syndrome) (table S1) and changes in pollinator preferences in the field (Table ane). In contrast, 2 studies of mating system isolation detected many smaller genetic changes (table S1). These different architectures might be explained by the fact that many intermediate pollinator syndromes are maladaptive (e.g., red flowers lacking a nectar advantage are unattractive to both birds and bees) and favor larger genetic steps, whereas small increases in selfing rates may exist favored if inbreeding depression costs are non prohibitive (14). Analyses of the direction of QTL furnishings imply that most traits contributing to prepollination isolation diverged through directional selection; equally predicted for adaptive phenotypes, QTL effects for these traits are mostly in the aforementioned management as the parental differences (15). QTL furnishings are predicted to vary in direction (i.east., take opposing effects) for traits not nether consistent directional option (16).

Contempo genetic analyses of prezygotic and extrinsic postzygotic barriers associated with detached habitat differences are particularly informative because many of the studies have been performed in the field. This makes it possible to estimate the strength of selection on traits and QTLs that contribute to habitat isolation. Studies have shown, for case, that the strength of selection on QTLs that contribute to habitat isolation is sufficient to permit speciation in the presence of gene flow, that hybrid inviability may arise as a by-product of habitat selection, and that interspecific hybridization tin facilitate the exchange of adaptive alleles between species (table S1).

Genetic studies of postpollination, prezygotic isolation have focused on the relationship between self-incompatibility (SI) mechanisms, which enforce outcrossing in many hermaphroditic plants, and interspecific incompatibility. This involvement stems from early on observations that cocky-compatible species are more than compatible in interspecific crosses than are SI species, implying that SI may contribute to both intra- and interspecific incompatibilities. This was confirmed past detection of a QTL for interspecific incompatibility that colocalizes with the SI locus, also as observations that crosses between cocky-compatible species fail later transformation with a SI factor from a self-incompatible species (table S1). Diversification of genes that contribute to SI appears to result from frequency-dependent selection (17). Interestingly, other institute reproductive proteins announced to be under positive selection as well, including candidates for species-specific recognition between pollen and stigma (table S1).

Intrinsic postzygotic barriers offer special challenges to genetic analyses because the phenotypes of interest (hybrid sterility and inviability) impede genetic study and lack obvious candidate genes for functional analyses (meet beneath, all the same). Intrinsic postzygotic isolation may be caused by chromosomal rearrangements and/or changes in genes (Fig. 1). Population genetic theory minimizes the importance of strongly underdominant chromosomal rearrangements (those that reduce the fitness of heterozygotes) because their negative effects on fitness should prevent them from condign established, except in small, inbred populations. Weakly underdominant rearrangements are more easily established simply contribute little to reproductive isolation. In dissimilarity, the Bateson-Dobzhansky-Muller (BDM) model accounts for the accumulation of interspecific incompatibilities in genes without loss of fettle (Fig. 1). Briefly, as a lineage diverges, geographically isolated or neighboring allopatric populations may accumulate independent mutations. These mutations are uniform with the ancestral genotype only are incompatible when combined. BDM incompatibilities generally involve 2 or more loci, although it is theoretically possible for BDM incompatibilities to result from the allopatric accumulation of independent mutations at a unmarried locus (Fig. 1).

Genetics of hybrid incompatibilities. (A) Example of a typical chromosomal rearrangement in plants, showing loss of fertility in heterozygotes because 50% of gametes are unbalanced genetically and inviable. (B) Classic two-locus BDM incompatibility in which new mutations are established at alternate loci and without loss of fettle in geographically isolated populations, but which are incompatible in hybrids. (C) Single-locus BDM incompatibility in which new mutations are established at the aforementioned locus and without loss of fettle in geographically isolated populations, but which are incompatible in hybrids.

Despite theoretical doubts about their importance in speciation, chromosomal rearrangements often contribute to the sterility of hybrid plants (18, 19). Different Drosophila (in which hybrid sterility is mostly due to BDM incompatibilities), sterile plant hybrids often recover fertility after chromosomal doubling (xviii). This is expected if chromosomal rearrangements are the cause of sterility, because chromosomal doubling furnishes an exact homolog for each chromosome, whereas doubling should not touch on BDM incompatibilities. Microchromosomal rearrangements such every bit the gain and loss of indistinguishable genes are more frequent than previously suspected and may atomic number 82 to hybrid incompatibilities with no loss of fitness in the diverging lineages (20). Finally, hybrid sterility in plants frequently maps to chromosomal rearrangements (21), although whether the cause is chromosomal underdominance or BDM loci that have accumulated within the rearrangements is often unclear. The reduced recombination associated with chromosomal rearrangements can facilitate the accumulation of hybrid incompatibilities in these regions (19, 22) or expedite the establishment of rearrangements in the first place (23).

BDM hybrid sterility in plants may exist under uncomplicated or circuitous genetic control. However, fewer loci contribute to hybrid sterility in plants than in Drosophila, and at that place appears to be no difference in the numbers of pollen (male person) versus seed (female person) incompatibilities, perhaps because plants largely lack differentiated sex chromosomes (24). In add-on, cytoplasmic male sterility examples characterized at the molecular level (26). CMS phenotypes are rescued by nuclear-encoded, mitochondrial-targeted genes that restore fertility (Rf genes). With the exception of Rf2 from maize, all cloned Rf genes are members of the pentatricopeptide repeat gene family (PPR), an unusually large gene family in plants (441 genes in Arabidopsis) that controls organelle gene expression. Although the molecular development of Rf genes is unknown, they are likely to be involved in coevolutionary chases with CMS as a result of genetic conflict between cytoplasmic and nuclear genes. These evolutionary dynamics may reduce the long-term effectiveness of CMS as a species barrier, because the same evolutionary forces that cause the spread of CMS within species could facilitate the introgression of CMS and restorers across species boundaries.

BDM factors also can crusade hybrid weakness or inviability. Hybrid weakness is often manifested every bit necrosis in developing seedlings or adult plant tissue, similar to the phenotype of pathogen attacks (27). These observations imply that hybrid weakness may outcome from changes in pathogen resistance genes (Table 1), which diverge in response to selection pressure exerted by pathogens. More studies are needed to determine the frequency of this machinery for hybrid (CMS), which results from an incompatibility between the institute'southward nuclear genome and its cytoplasm, is ofttimes reported in intra- and interspecific plant hybrids, but non in animal hybrids (25). CMS is under frequency-dependent selection in hermaphrodite-biased populations, which predominate in plants, but under strong negative option if at that place are separate male and female sex activity morphs. CMS is acquired past aberrant, frequently chimeric, mitochondrial genes in all weakness in interspecific crosses and to elucidate other mechanisms of hybrid inviability.

A terminal emerging divergence betwixt plants and animals (or at to the lowest degree Drosophila) is that most BDM incompatibilities characterized in plants are polymorphic within species (27–29) (Table i ). This is consequent with an origin of BDM incompatibilities through frequency-dependent selection, local accommodation, or migrate. However, information technology also implies that BDM incompatibilities are rarely the cause of speciation in plants, considering they correlate poorly with species boundaries and typically brand small contributions to total isolation.

Hybrid and Polyploid Speciation

Although virtually studies of speciation focus on how lineages diverge, speciation is non ever most divergence. Indeed, a substantial fraction of speciation events in plants involves the reunion of divergent genes and genomes through sexual hybridization. There are 2 kinds of hybrid speciation: homoploid and polyploid. Homoploid hybrid speciation refers to the origin of a new hybrid lineage without a alter in chromosome number, whereas polyploid hybrid speciation involves the total duplication of a hybrid genome (allopolyploidy). Polyploids not of hybrid origin are autopolyploids.

Homoploid hybrid speciation is rarer than polyploid speciation for two reasons. First, homoploid hybrid species have strongly reduced fitness in early generation hybrids equally pick eliminates incompatibilities. In dissimilarity, polyploid species need not accept low fertility during intermediate stages. Second, genome duplication protects the genetic integrity of newly derived polyploids, merely no such bulwark prevents homoploid hybrids from back-crossing with their parental species. In add-on to these biological difficulties, homoploid hybrid species are technically challenging to observe because they often lack diagnostic features, such as a modify in chromosome number. And then far, in that location are 15 to 20 good examples in the literature (30), but more are likely to be discovered with the widespread application of genomic tools to natural found populations (31).

Homoploid hybrid species may become reproductively isolated by rapid karyotypic development, ecological divergence, and spatial isolation of the new hybrid lineage. Simulation studies indicate that although strong ecological selection promotes hybrid speciation, without chromosomal or spatial isolation the hybrid population forms a steep step in a cline betwixt the parental species (32). Karyotypic divergence and spatial isolation both reduce the probability that hybrid species will be generated but volition enhance the evolutionary independence of hybrid lineages once they ascend.

As hypothesized, all establish homoploid hybrid species are ecologically diverged and exhibit some degree of ecogeographic isolation, and roughly one-half have differing karyotypes (30). Most normally, the hybrid species are adjacent to i or both parental species, although in that location are examples of long-altitude dispersal also (table S1). Some hybrids occupy habitats that are intermediate between the parental species, whereas others have colonized an extreme addiction by combining QTLs with effects in the same direction from both parental species (Tabular array i and Fig. ii). Homoploid hybrid species are hands recreated in the greenhouse, perhaps explaining why many are multiply derived in the wild (tabular array S1).

Genetic basis of transgressive segregation showing how segregating hybrids can combine plus and minus alleles from parental species, thereby generating extreme phenotypes or adaptations to extreme habitats.

In contrast to homoploid hybrid species, polyploid species are easily diagnosed considering of chromosome number changes associated with genome doubling. However, the frequency of polyploid speciation remains controversial. When there are multiple polyploid species inside a genus, it is difficult to determine whether there was a unmarried transition to the new ploidal level followed past divergent speciation or whether each polyploid species arose independently. Contempo model-based estimates (33) assume a single transition to a new ploidal level within a genus and provide a lower bound of the polyploid speciation charge per unit: 2 to 4% in flowering plants and 7% in ferns. This contrasts with Stebbins' (34) estimate of 30 to 35% for flowering plants, which assumes that all polyploid species within a genus are independently derived. Because many polyploid species are themselves multiply derived (Table i), Stebbins' estimate is probably closer to the true polyploid speciation rate. Nevertheless, neither of these estimates (33, 34) includes intraspecific ploidal variation. At least 8 to 9% of named plant species vary in ploidal level, and this might be the tip of the iceberg (35). If each ploidal level (cytotype) is viewed as a cryptic biological species, then the contribution of polyploidy to biological species diversity is fifty-fifty college than previously surmised. In improver, in that location has been defoliation betwixt estimates of the proportion of species that are polyploid and the rate of polyploid speciation. Analyses of the age distribution of duplicate genes in diverse flowering plants (36) betoken that essentially all may be paleopolyploids, simply this should not be equated with the polyploid speciation rate.

Polyploids can arise by somatic doubling, by the fusion of unreduced gametes, and by means of a triploid bridge (Fig. 3). Unreduced gametes are common in plants and probable represent the near frequent route to polyploidy (37). Nevertheless, most newly arisen polyploids neglect to become established because of meiotic abnormalities and/or the paucity of advisable mates (38). The establishment of polyploids is favored by differential niche preference, low dispersal, a selfing or asexual mating system, high fecundity, and a perennial life history (39, 40). Niche separation, depression dispersal, and selfing increase the probability of successful matings during early stages of polyploid species institution; otherwise most matings volition exist with the diploid progenitors (xl, 41). Stochastic events due to a pocket-size number of polyploid colonizers subtract the chance of institution, but this barrier is minimized past high fecundity and a perennial life history, which allows plants to reproduce at multiple times over their life cycle (39).

Mechanisms by which polyploids tin arise. (A) Somatic doubling, in which chromosome number is doubled in vegetative tissue that gives rise to reproductive organs. (B) Fusion of unreduced gametes that are produced when cell walls fail to grade in the final stage of meiosis. (C) A triploid span, in which unreduced and reduced gametes form triploids. If the triploids also produce unreduced gametes, the triploid gametes may fuse with reduced gametes from diploid individuals to generate stable tetraploids.

Because intraspecific matings are far more than common than interspecific matings in natural populations of plants, autopolyploids must ascend at a much higher rate than allopolyploids (37). However, named species are more likely to be allopolyploids (42), which implies that allopolyploids are more than easily established in nature, easier to find, and/or more readily recognized by taxonomists. Establishment of allopolyploids is favored because of greater niche separation from their diploid progenitors (43), and taxonomists appear reluctant to name phenotypically cryptic autopolyploid species.

Recent attending has been given to changes in gene expression, genome content, and DNA methylation that accompany hybrid and polyploid speciation, but these genomic alterations only rarely accept been linked to changes in ecology or mating organization that touch on polyploid institution (Table 1). Indeed, many described genomic changes appear to be maladaptive past-products of reuniting divergent genomes. However, maladaptive changes in cistron expression in outset-generation interspecific hybrids may be reduced by genome doubling, and elimination of DNA sequences may aid restore fertility in polyploids (table S1).

Factors Affecting Speciation or Extinction Rates

Recent advances in comparative methods take made it possible to identify biological or geohistorical factors affecting speciation or extinction rates. The most rigorous approach compares species richness of multiple sister clades that differ in the presence or absenteeism of a given trait (44). A significant association may outcome from either increased speciation or reduced extinction. Traits associated with increased species richness in plants include resin canals, nectar spurs, biotic pollination, herbaceous growth form, abiotic dispersal, increased neutral development, bilateral symmetry of flowers, twig epiphytism, and polyploidy (45) (table S1). Many of these examples involve biotic interactions, leading to suggestions that coevolution may drive speciation in many plant groups or that niche infinite may be less constrained in biotic than abiotic interactions (46). The nigh rapid diversification rates in plants are associated with ecological opportunities created by major geological changes such as the uplift of the Andes or isle formation (Table 1), which implies that mechanisms that aggrandize niche multifariousness oftentimes increment species diversification (or reduce extinction). Unfortunately, the factors listed in a higher place do non fully business relationship for the near hitting trend in species richness—the negative correlation with breadth—which appears to accept a pluralistic explanation (47) (tabular array S1).

Concluding Remarks

The field of constitute speciation is in for an heady decade. The wide availability of genomic tools and resources for crop and noncrop species, from light-green algae to mosses to angiosperms, will accelerate our understanding of the genetic and ecological bases of speciation. These resource not but will facilitate the cloning and functional characterization of genes underlying reproductive barriers merely too will brand it possible to quantify the effects of individual mutations or alleles on reproductive isolation or fitness in natural populations (Table 1). Likewise, the widespread application of molecular phylogenetic approaches simplifies comparative report.

Nosotros wait to see rapid progress in each of the areas highlighted in our review. For example, studies of the geography of selective sweeps should provide an objective method for evaluating the importance of different kinds of reproductive barriers and geohistorical processes in speciation. Our agreement of reproductive isolation will also exist enhanced by boosted field-based estimates of isolation beyond all life history stages. With the cloning of BDM incompatibilities in plants, the next step is molecular evolutionary studies of these genes to identify the forces that drive their evolution. Finally, comparative analyses of the effects of unlike kinds of reproductive barriers on species richness should allow usa to decide whether reproductive barriers themselves increment speciation rates.

Footnotes

References and Notes

i. Arnold ML. Natural Hybridization and Evolution. Oxford Univ. Press; Oxford: 1997. [Google Scholar]

2. Mishler BD, Donoghue MJ. Syst Zool. 1982;31:491. [Google Scholar]

ix. Ramsey J, Bradshaw Hard disk, Schemske DW. Evolution Int J Org Evolution. 2003;57:1520. [PubMed] [Google Scholar]

10. Stebbins GL. Variation and Development in Plants. Columbia Univ. Press; New York: 1950. [Google Scholar]

xiv. Fishman Fifty, Kelly AJ, Willis JH. Evolution Int J Org Evolution. 2002;56:2138. [PubMed] [Google Scholar]

20. Werth CR, Windham Dr.. Am Nat. 1991;137:515. [Google Scholar]

25. Fishman L, Willis JH. Evolution Int J Org Evolution. 2006;threescore:1372. [PubMed] [Google Scholar]

26. Gillman JD, Bentolila S, Hanson MR. Plant J. 2007;49:217. [PubMed] [Google Scholar]

28. Christie P, Macnair MR. Development Int J Org Evolution. 1987;41:571. [PubMed] [Google Scholar]

29. Sweigart AL, Mason AR, Willis JH. Evolution Int J Org Development. 2007;61:141. [PubMed] [Google Scholar]

32. Buerkle CA, Morris RJ, Asmussen MA, Rieseberg LH. Heredity. 2000;84:441. [PubMed] [Google Scholar]

34. Stebbins GL. Chromosomal Development in College Plants. Edward Arnold; London: 1971. [Google Scholar]

35. Soltis DE, et al. Taxon. 2007;56:thirteen. [Google Scholar]

37. Ramsey J, Schemske DW. Annu Rev Ecol Syst. 1998;29:467. [Google Scholar]

41. Rausch JH, Morgan MT. Development Int J Org Evolution. 2005;59:1867. [PubMed] [Google Scholar]

44. Hodges SA, Arnold ML. Proc R Soc London B Biol Sci. 1995;262:343. [Google Scholar]

45. Coyne JA, Orr HA. Speciation. Sinauer Assoc; Sunderland, MA: 2004. [Google Scholar]

46. Bolmgren K, Eriksson O, Linder HP. Evolution Int J Org Development. 2003;57:2001. [Google Scholar]

48. Nagy ES, Rice KJ. Evolution Int J Org Evolution. 1997;51:1079. [PubMed] [Google Scholar]

55. We give thanks the great botanical naturalists of the 20th century who provided the foundation for electric current studies of found 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. Nosotros also thank members of the Rieseberg and Willis laboratories and three referees for useful comments on an before version of this newspaper. The authors' research on speciation has been supported by NSF, NIH, USDA, and the National Sciences and Engineering Research Council of Canada.

Source: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2442920/

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