Ecology of plant speciation

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Abstract:

Ecology affects each of the three principal processes leading to speciation: genetic differentiation among populations within species, acquisition of reproductive isolation among populations, and the rise of ecological differentiation among such populations, allowing them to coexist. Until recently, however, the ties between ecology and speciation in plants have received relatively little attention. This paper reviews some exciting new insights into the role of ecology in speciation, focusing on the angiosperms. I consider five main topics, including (1) the determinants of the spatial scale of genetic differentiation within species; (2) the role and limits of adaptive radiation in increasing net rates of plant diversification; (3) the potential role of ecological speciation; (4) the contributions of hybridization to speciation, adaptive radiation, and the ecological breadth of clades; and (5) the ecological determinants of net diversification rate for individual lineages, and of the species richness for regional floras.

Limited dispersal, especially of seeds, favors genetic differentiation at small spatial scales and is likely to foster rapid speciation and narrow endemism. Meta-analyses show that the minimum area required for in situ speciation on islands increases with the spatial scale of gene flow in various organisms. In angiosperms, fleshy fruits dispersed by vertebrates often increase the distance over which seeds are dispersed, but can decrease it in forest understories. Nutrient-poor soils should work against the evolution of fleshy fruits and promote speciation and narrow endemism.

Selection for adaptation to different conditions drives adaptive radiation, the rise of a diversity of ecological roles and attendant adaptations within a lineage. On islands, adaptive radiation often leads to woodiness, monocarpy, developmental heterophylly, and sexual dimorphism, as well as differences in habitat, growth form, and floral morphology. Adaptive radiation appears to accelerate speciation in only some plant clades. Extensive radiation in some lineages has been ascribed to early colonization, large amounts of heritable genetic variation, “genetic lines of least resistance” upon which selection could act, absence of potential competitors, and possession of “key innovations” that provide access to novel resources. To these should be added large island area, organismal abundance, saturation of ecological space, and the synergism action of limited dispersal and divergent selection producing parallel radiations in isolated regions. Data for Hawaiian lobeliads suggest that within-island species richness of Cyanea—involving divergence in elevation and flower tube length—saturates within 0.6 and 1.5 Ma.

Adaptive radiation in pollinators is an important mechanism of ecological speciation: adaptation to different pollinators leads to pollinator partitioning and reproductive isolation. Selection for longer nectar spurs and pollinator mouth parts led to increased speciation in Aquilegia and other groups. A similar process may work once tubular flowers evolve from cup-shaped blossoms. Selection for floral divergence may be limited in forest understories illuminated by dim, greenish light, which may account for the predominance of small, visually inconspicuous flowers in temperate and tropical understory species.

Hybridization can stimulate speciation by forming transgressive phenotypes that exceed the range seen in parental taxa, and by introgressing adaptive gene combinations. The likelihood of transgressive phenotypes increases with the genetic divergence between parental taxa, so speciation via transgressive hybridization may be most likely among taxa with intermediate amounts of divergence. Several large adaptive radiations appear to have occurred after hybridization, suggesting a special role for the extensive amount of genetic variation that can be supplied and refreshed by syngameons.

Rates of net species diversification are greater in herbs (especially annuals) vs. woody plants; in animal- vs. wind-pollinated species; in plants with poorly dispersed seeds; in families with a greater diversity of growth forms, pollination and seed dispersal mechanisms, and species distributions; in families at lower latitudes; in families with higher rates of genetic evolution; in hermaphroditic or monoecious vs. dioecious clades; in earlier-maturing woody plants; in plants with bilateral vs. radial flowers; in plants with hummingbird-pollinated flowers; in epiphytic vs. terrestrial bromeliads and orchids; in bromeliads differentiating along geographically extensive cordilleras; and in young vs. old clades. Evidence for the last pattern may, however, be an artifact of (auto)regressing (ln N) / t vs. t. High rates of diversification in epiphytic orchids are tied to small effective population sizes, suggesting a role for intermittent genetic drift alternating with strong selection on floral traits. Across angiosperms, a massive increase in diversification rates was preceded by a major increase in leaf vein density and hydraulic conductance between 140 and 110 Ma ago, leading to higher photosynthetic rates than coexisting ferns and gymnosperms. Based on the economic theory of plant defense, this should have led to lower allocation to anti-herbivore defenses, selecting for low-cost qualitative toxins rather than all-purpose but highly expensive qualitative defenses, triggering an arms' race between angiosperm and their herbivores. Finally, regional plant species richness increases with regional area and proxies for latitude, rainfall, topographic heterogeneity, and vegetation stratification. The Cape Floristic Province has roughly twice as many species as expected from its area and environmental conditions, most likely reflecting the predominance of short-distance dispersal associated with poor soils and myrmecochory in the Cape Province, as well as low rates of regeneration and competitive exclusion following fire.

Keywords: ADAPTIVE RADIATION; DIVERSITY; GENETIC STRUCTURE; SEED DISPERSAL; TRANSGRESSIVE HYBRIDIZATION

Document Type: Research Article

Publication date: October 1, 2010

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