Natural Selection and Ecological Speciation in Sticklebacks

The idea that selection may be fundamental to the origin of species dates back at least to the synthesis of modern evolutionary theory, being present in the writings of Fisher (1930), Muller (1942), and Dobzhansky (1951). Nevertheless, despite almost three-quarters of a century since the idea was first proposed, little progress has been made in testing the role of selection in speciation (Coyne 1992; Schluter 1996a, 2001; Futuyma 1998). As the various chapters of this volume attest, however, the topic is enjoying a resurgence of interest (see also Schluter 2001). The purpose of this chapter is to summarize tests for the role of selection in speciation in a natural system: the sympatric populations of limnetic and benthic threespine sticklebacks that inhabit postglacial lakes in British Columbia, Canada (Plate 2). Our investigation specifically addresses the role of divergent selection between environments and niches in the origin of reproductive isolation, and the role of reinforcement in its completion. Throughout, we adopt Mayr’s (1942) biological species concept, in which species are groups of actually or potentially interbreeding natural populations that are isolated reproductively from other such groups. We broaden this definition slightly to recognize that imperfect reproductive isolation can exist between species that nevertheless maintain their distinctiveness in nature (Rundle et al. 2001). We focus on the question of “ecological speciation”, a term that encompasses various speciation scenarios in which divergent natural selection between niches or environments is ultimately responsible for the evolution of reproductive isolation (Box 9.1). Ecological speciation differs from adaptive speciation as defined in Chapter 1 in two ways (Boxes 1.1 and 19.1). First, ecological speciation can also occur in allopatry (Box 9.1) and, second, ecological speciation does not include cases in which disruptive selection and subsequent divergences result entirely from sexual selection. Ecological speciation includes cases in which reproductive isolation evolves wholly as an indirect by-product of adaptation to alternative resources and environments, as well as several mechanisms in which natural selection directly favors the evolution of reproductive isolation (Box 9.1). Later we attempt to determine whether, in the stickleback speciation process, direct natural selection has played a role. Speciation by sexual selection is also ecological speciation if divergent natural selection between environments drives divergence in mate preferences, leading to reproductive isolation (Schluter 2000).