Beyond dichotomies in species and speciation

Speciation is not as mysterious as Darwin once described it [1]. Nevertheless, important questions remain. As discussed by Wu [2] and highlighted in a series of papers in National Science Review (NSR), these issues equate with imposing dichotomous perspectives on speciation, when the nature of species and the processes creating them can complicate discrete categorization. The question of what constitutes a species has a long, contentious history [3,4]. Inherent barriers to gene flow can generate increasing phenotypic, genetic and reproductive gaps between populations with time. However, defining when these gaps are sufficient to recognize ‘distinct’ species—rather than partly separated ecotypes or races—may be subjective unless reproductive isolation (RI) is complete. Consequently, Wu [2] notes, researchers delineate species differently in relation to their objectives. Thus, one may consider species as an artificial taxonomic category not different from a genus, as Darwin [1] did, despite viewing the gaps between species as real. With respect to delineating species, Wu [2] uses the analogy of changing seasons. Earlier, Walsh [5] compared the problem to the transition from childhood to adulthood. In the analogies of Wu and Walsh, however, non-arbitrary demarcations can be made in terms of changes in day length and sexual maturity, respectively. The issue then is: does speciation usually proceed in ‘fits and bursts’, transitioning between identifiable phases recognizable as populations versus species or gradually, producing a continuum of forms not easily or universally categorized [6–8]? The answer may sometimes be ‘yes’ and other times ‘no’ (e.g. see work on Heliconius butterflies [9]; and on mangroves [10], glacial fish [11], Rhododendron plants [12] and marine diversity [13] in this issue of NSR). In one of our study systems, Timema stick insects, there is a clear break in genomewide differentiation such that only modest (FST < 0.30) and high (FST > 0.70) levels of differentiation occur in sympatry, interpretable as populations versus species [14]. Notably, this ‘gap’ is not seen in allopatry, where differentiation between populations gradually blends into that between species, demonstrating the context-dependent nature of divergence. In another of our study systems,Rhagoletis fruit flies, a break in differentiation in sympatry is not obvious [15]. For Rhagoletis, where speciation is often initiated by divergent ecological selection associated with host plant shifts, species may represent host races writ large [16]. This does notmean, however, that species cannot still be statistically defined, for instance, by the degree to which they form distinct genotypic clusters or can be correctly assigned to oneor anotherhost taxon [4,17,18]. Thechallenge then is equating these probabilistic definitions of species with the process of speciation. Groups displaying distinct gaps compared to those that do not may reflect important differences in their natural histories (e.g. the role of ecology), population genetics (e.g. the strength of selection and effect sizes of mutations versus migration and recombination rates), and biogeography (e.g. the geographic context of divergence and how it changes, effecting gene flow and standing variation through time) that are responsible for these patterns and seminal to understanding the speciation process. Thus, the use of any given species definitions may be somewhat subjective andbemore representative of one phase of divergence than others [19]. However, this does not mean that these definitions do not embody some underlying biological reality with respect to process and thus can be useful for understanding species formation. In NSR, Orr et al. [20] offer suggestions to attempt to standardize the taxonomic problem of species. While they do not provide criteria for objectively defining species, they propose a checklist of data to collect in order to help unify the delineation of taxa. The utility of this endeavor is that any researcher armed with this holistic data set could, in principle, reach the sameconclusion regarding species status for a given specificdefinition.Thus, if phases of speciation canbe equatedwith different species definitions [6–8,19], then this could aid greatly in better understanding the relationship of pattern and process in speciation. Defining species could be described as an attempt to dichotomize patterns of divergence into distinguishable and named categories of biodiversity. With respect to process, speciation has also been dichotomized into categories based on underlying causal factors. A short list includes: