A Shift in Focus

Millions of species currently exist on earth, and to secure an understanding of how all this magnificent variety arose is no small task. Biologists have long accepted Darwinian selection as the central explanation of adaptation and evolutionary change; yet, to date, no similar agreement has emerged about evolutionary processes that can create two species out of one. Almost 150 years after Darwin's seminal work On the Origin of Species (1859), conditions for and mechanisms of biological speciation are still debated vigorously.

The traditional “standard model” of speciation rests on the assumption of geographic isolation. After a population has become subdivided by external causes – like fragmentation through environmental change or colonization of a new, disconnected habitat – and after the resultant subpopulations have remained separated for sufficiently long, genetic drift and pleiotropic effects of local adaptation are supposed to lead to partial reproductive incompatibility. When the two incipient species come into secondary contact, individuals from one species cannot mate with those of the other – even if they try – or, if mating is still possible, their hybrid off spring are inferior. Further evolution of premating isolation (like assortative mate choice or seasonal isolation) and/or postmating isolation (like gametic incompatibility) eventually ensures that the two species continue to steer separate evolutionary courses.

The trigger for speciation in this standard model is geographic isolation. It is for this reason that the distinction between allopatric speciation (occurring under geographic isolation) and sympatric speciation (without geographic isolation) has taken center stage in the speciation debate.

Introduction

The term “phylogeography” was introduced by Avise (Avise et al. 1987) to refer to the principles and processes that govern the geographic distributions of genealogical lineages, including those at the intra-specific level (Avise 1994). Since then, the use of DNA markers to study phylogeography has become very popular, with an increasing flood of studies on a diverse range of taxa. The data from these studies are interpreted traditionally within the framework of limited dispersal (isolation by distance) or past vicariance events (isolation by geographic barriers), considered against the geographic and geologic history of the area under study. The resultant patterns are then discussed in the context of passive divergence and are taken as evidence for allopatric speciation scenarios. However, the argument presented here is that at least some of these patterns could also be seen in a different light and might provide evidence for sympatric modes of speciation.

The crucial point in this context is that the consequences of assortative mating should be considered for the generation of patchy distribution patterns, as well as for the maintenance of borders between the patches. The evolution of assortative mating is generally an integral part of sympatric speciation models, both for the ecologically driven ones (Rice 1987; Doebeli 1996a; Johnson et al. 1996b; Dieckmann and Doebeli 1999; Kondrashov and Kondrashov 1999) and for those based on sexual selection (Turner and Burrows 1995; Higashi et al. 1999). In general, assortative mating amounts to an avoidance of hybridization under contact conditions.

Theories of speciation, in the past often couched in verbal terms, should explain how ecological divergence and genetically determined reproductive isolation evolve between lineages that originate from single, genetically homogeneous ancestral populations. As Will Provine highlights in Chapter 2, the predominant perspective for a long time was that reproductive isolation emerges as a by-product of other evolutionary processes, through the incidental accumulation of genotypic incompatibility between related species. It is easiest to imagine that such incompatibilities arise when subpopulations become geographically isolated and henceforth evolve independently: genetic distance between them is then expected to increase with time. Thus, “given enough time, speciation is an inevitable consequence of populations evolving in allopatry” (Turelli et al. 2001). On a verbal level this theory of allopatric speciation appears both simple and convincing. This apparent theoretical simplicity has contributed to the view that the allopatric mode of speciation is the prevalent one – a perspective that has found its most prominent advocate in Ernst Mayr (Chapter 2).

Unfortunately, not only is the simplicity of the usual accounts of allopatric speciation based on the poorly understood concept of genetic incompatibility, but simplicity in itself is no guarantee for ubiquitous validity. Other plausible, but theoretically more intricate, mechanisms for the evolution of reproductive isolation in the absence of geographic isolation have been proposed. Recent approaches have focused attention on adaptive processes that lead to ecological and reproductive divergence as an underlying mechanism for speciation processes – a change in emphasis that occurred concomitantly with a shift in biogeographic focus from allopatric scenarios to parapatric speciation between adjacent populations or fully sympatric speciation. This was foreshadowed by the idea of reinforcement (the evolution of prezygotic isolation through selection against hybrids) and has culminated in theories of sympatric speciation, in which the emergence and divergence of new lineages result from frequency-dependent ecological interactions.

When Terry Erwin from the Smithsonian National Museum of Natural History examined the diversity of beetles that lived on a single species of tropical trees, he found 682 different beetle species, 163 of which he classified as specialist species that lived exclusively on the particular tree species used in his study. Since there are around 50000 tropical trees species, Erwin extrapolated that there must be on the order of 7 million specialist beetle species (Erwin 1982). Using similar extrapolations, Erwin (1982) also estimated the total number of tropical arthropod species as about 30000000. While these estimates may be too high (Schilthuizen 2000; Ødegaard 2000; Novotny et al. 2002), they are mind-boggling nevertheless and serve as an illustration of the incredible amount of species diversity that exists on our planet: estimates for the total number of extant species of plants and animals range from 10 million to 100 million (May 1990; Schilthuizen 2000). It is also estimated that the number of extant species represents only about 1% of the total number of species that ever existed during the history of life on earth. Together with the common phylogenetic ancestry usually inferred for the tree of life for higher organisms, this implies that speciation must have been truly rampant during the creation and evolution of our biosphere.