The rise and fall of plant species: a population biologist's perspective

These are exciting times for plant evolutionary biology. Molecular data, new analytical techniques, and thoughtful experiments and syntheses are providing insights into many classic issues, including phylogeny and character-state evolution at every taxonomic level (e.g., Barrier et al., 1999; Panero et al., 1999; Soltis et al., 2000a, b; Pryer et al., 2001; Sytsma and Hahn, 2001), patterns of adaptive radiation (Givnish and Sytsma, 1997a; Les, Cleland, and Waycott, 1997; Baum, Small, and Wendel, 1998), the history of geographic differentiation within and among species (Wagner and Funk, 1995; Wen, 1999; Abbott et al., 2000; Givnish et al., 2000; Schaal and Olsen, 2000; Wright et al., 2000), gene flow and spatial scales of genetic differentiation within and among populations (Wolf and Soltis, 1992; Hamrick, Murawski, and Nason, 1993; Nason, Herre, and Hamrick, 1998; Cain, Milligan, and Strand, 2000), the impacts of hybridization and polyploidy on speciation, adaptation, gene expression, and chromosomal evolution (Arnold, 1997; Rieseberg, 1997; Burke, Voss, and Arnold, 1998; Cook et al., 1998; Husband and Schemske, 1998; Brubaker, Patterson, and Wendel, 1999; Cronn, Small, and Wendel, 1999; Rieseberg, Baird, and Gardner, 2000; Soltis and Soltis, 2000), the concordance of genomic architecture among closely related taxa (Moore et al., 1995; Wendel, 2000), the genetic bases for reproductive isolation via specialization on different pollinators (Bradshaw et al., 1998; Schemske and Bradshaw, 1999), and the genetic evolution of certain key aspects of floral development (Meyerowitz, 1994; Doebley and Wang, 1997; Albert et al., 1998; Baum, 1998; Bowman et al., 1999). Given these remarkable developments, and the three decades that have elapsed since the last comprehensive-and magisterial-treatments of plant speciation and evolution by Grant (1971) and Stebbins (1971, 1974), it was with the greatest interest that I awaited Don Levin's new book The Origin, Expansion, and Demise of Plant Species. Levin was a hero of my youth, who had made his name in plant population biology, but also added substantially to our understanding of speciation through his research on the genus Phlox (Polemoniaceae). His contributions included early studies of plant demography, genetic differentiation among populations, divergence in pollination biology among closely related species, selection for reproductive isolation, and constraints on species ranges. Levin's intriguing premise is that we can best understand plant evolution if we view plant species as having a life cycle, from birth to geographic expansion, genetic differentiation and diversification, increasing disunity, and ultimately death through extinction. Levin argues that the evolutionary trajectory taken by each species should depend on the nature and organization of its genetic variation, its dispersal ability, and ecological interactions with competitors, predators, and mutualists, and the habitats it encounters, but that, nevertheless, different species should show several similarities if they occupy a similar life-cycle stage. After birth, species should rapidly acquire genetic variation, expand in range, and undergo genetic differentiation; aging should be manifested by the contraction and/or fragmentation of geographic range, loss of genetic variation, and increased likelihood of extinction. The evolutionary trajectory taken by a species should depend on its own genetic and ecological attributes, as well as its interactions with a changing physical and biological environment. Levin thus asserts that ecological issues must take equal place with the genetic ones traditionally considered if we are to understand the evolution of species. This proposal makes good sense: ecology helps determine the nature of the initial divergence of species from their progenitors, sets the stage for subsequent adaptive evolution, imposes constraints on gene flow and thus speciation rates, subsequent range expansion, and geographic differentiation, and saddles species with an ever-increasing burden of competitors, herbivores, pests, and developmental and genetic constraints. The nature of genetic variation, in turn, helps determine a species' response to these ecological pressures. Levin develops these themes through nine chapters, devoted to (1) the historical framework just given and a brief review of species concepts, (2) the ecological bases of speciation, (3) the genetic bases of speciation, (4) the geographic scale of speciation, including a critique of traditional models of geographic speciation, (5) range expansion and species limits, (6) genetic differentiation and the loss of cohesion through the formation of ecological and chromosomal races, (7) species decline and extinction, (8) the ecological and genetic mechanisms by which existing species may interfere with the rise and further evolution of incipient species, and (9) species' longevities and how they may vary with ecological conditions. The book is a review and synthesis of previously published work, with almost no new data, concepts, or overarching theories developed for the book itself. Chapters begin with a brief statement of Levin's views of the ecological and/or genetic issues involved in a particular topic, followed by a lengthy enumeration of empirical findings supporting this perspective, and concluding with a short overview. While exciting in prospect, Levin's magnum opus is, alas, a serious disappointment in its realization. We immediately get into deep water in Chapter 1 with a baffling discussion of species concepts, a fundamental issue for any book with the ambition to reshape our views on plant speciation. Even though this subject has been treated incisively by Mayr, Stebbins, Grant, and many other luminaries-and even though Levin cites these authors as well as recent symposia (e.g., Howard and Berlocher, 1998) that vividly capture the vigor and rigor of current debate-Levin's treatment is the least