Ecology. Michael Begon

Figure 1.10 Closure of a ring distribution of bulbul morphotypes. (a) Distribution of Alophoixus bulbuls in the Indo‐Malayan bioregion. Taxa composing the Alophoixus ring are represented by circles (colours distinguish three currently recognised species); single arrows represent colonisation around the barrier; double arrows represent zones of genetic intergradation; closure of the ring (involving taxa 1 and 7) is shown at the top left (the question mark indicates a possible secondary contact at the mid‐ring involving taxa 5 and 7). (b) Eco‐morphotypes: (1) A. flaveolus, (2) A. ochraceus ochraceus, (3) A. o. cambodianus, (4) A. o. hallae, (5) A. pallidus khmerensis, (6) A. p. annamensis and (7) A. p. henrici.

      Source: From Fuchs et al. (2015), after Pereira & Wake (2015). (b) Photo credit: A. Previato, MNHN.

      allopatric speciation without secondary contact

      It would be wrong to imagine that all examples of speciation conform fully to the orthodox picture described in Figure 1.8. In fact, there may never be secondary contact. This would be pure ‘allopatric’ speciation; that is, with all divergence occurring in subpopulations in different places. This seems particularly likely for island populations and helps explain the preponderance of endemic species (those found nowhere else) on remote islands.

      1.3.3 Sympatric speciation

Furthermore, the advent of modern molecular techniques has spurred interest in the view that an allopatric phase may not be necessary: that is, ‘sympatric’ speciation is possible, with subpopulations diverging despite not being geographically separated from one another. Sympatric speciation has long fascinated evolutionary biologists because it sets diversifying selection against the tendency of sexual reproduction to homogenise populations. There are few truly convincing cases in nature, and indeed it is to be expected that examples of such a process will be difficult to identify because, for most groups, range maps are incomplete, the patterns of habitat use are poorly known and phylogenies do not include all species (Santini et al., 2012). Once again, however, mathematical models provide a way of testing the viability of alternative speciation scenarios and suggest the criteria that need to be satisfied (Bird et al., 2012). There are at least five criteria for inferring that a particular case is best explained by sympatric speciation – four proposed by Coyne and Orr (2004): (1) the two species must have largely overlapping geographical distributions; (2) speciation must be complete; (3) the two species must be sister species (descended from a common ancestor); and (4) the biogeographic and evolutionary history of the groups must make the existence of an allopatric phase ‘very unlikely’; and a fifth, based on a population genetics rather than biogeographic perspective: (5) evidence must support panmixia of the ancestral population (i.e. mating must have been possible between all potential partners) (Fitzpatrick et al., 2008.

A good example is provided by two species of cichlid fish in Nicaragua: the Midas cichlid Amphilophus citrinellus and the arrow cichlid A. zaliosus (Figure 1.11a) (Barluenga et al., 2006). These species coexist in the small, isolated Lake Apoyo (satisfying criterion 1), which is relatively homogeneous in terms of habitat, and of recent origin (less than 23 000 years). A. zaliosus is found nowhere else, while A. citrinellus occurs in many water bodies in the region, including the largest. A variety of behavioural (mate choice) and genetic evidence, including that from microsatellite DNA, indicates that the two species in Lake Apoyo are reproductively isolated from one another (satisfying criterion 2) and indeed from A. citrinellus in other lakes (Figure 1.11b). Further genetic evidence from mitochondrial DNA (passed by mothers to their offspring) indicates that the cichlids of Lake Apoyo, of both species, had a single common ancestor arising from the much more widespread stock of A. citrinellus (Figure 1.11c) (satisfying criteria 3 and 5). The common ancestor was a high‐bodied benthic species but A. zaliosus, the new elongated pelagic species, has evolved in less than 10 000 years. Now A. citrinellus and A. zaliosus in Lake Apoyo are morphologically distinct from one another and have substantially different diets: both feed on biofilm but A. citrinellus feeds more from the benthic environment (algae, insects and fish along the lake shore and bed) while A. zaliosus feeds more from open water and the surface (including winged insects; Figure 1.11d). There seems little doubt, therefore, that this speciation must have occurred sympatrically, presumably driven by the divergent selection to specialise on bottom‐feeding in the one case and on open water‐feeding in the other.