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Allopatric speciation is speciation driven by divergent natural selection in distinct subpopulations in different places. The most orthodox scenario for this comprises a number of stages (Figure 1.8). First, two subpopulations become geographically isolated and natural selection drives genetic adaptation to their local environments. Next, as a byproduct of this genetic differentiation, a degree of reproductive isolation builds up between the two. This may be ‘pre‐zygotic’, tending to prevent mating in the first place (e.g. differences in courtship ritual), or ‘post‐zygotic’: reduced viability, perhaps inviability, of the offspring themselves. Then, in a phase of ‘secondary contact’, the two subpopulations re‐meet. The hybrids between individuals from the different subpopulations are now of low fitness, because they are literally neither one thing nor the other. Natural selection will then favour any feature in either subpopulation that reinforces reproductive isolation, especially pre‐zygotic characteristics, preventing the production of low‐fitness hybrid offspring. These breeding barriers then cement the distinction between what have now become separate species.

Figure 1.8 The orthodox picture of ecological speciation. A uniform species with a large range (1) differentiates (2) into subpopulations (for example, separated by geographic barriers or dispersed onto different islands), which become genetically isolated from each other. (3) After evolution in isolation they may meet again, when they are either already unable to hybridise (4a) and have become true biospecies, or they produce hybrids of lower fitness (4b), in which case evolution may favour features that prevent interbreeding between the ‘emerging species’ until they are true biospecies.

Darwin’s finches

The isolation of islands provides arguably the most favourable scenario for populations to diverge into distinct species. The most celebrated example is the case of Darwin’s finches in the Galápagos archipelago, a group of volcanic islands isolated in the Pacific Ocean about 1000 km west of Ecuador and 750 km from the island of Cocos, which is itself 500 km from Central America (Figure 1.9). At more than 500 m above sea level the vegetation is open grassland. Below this is a humid zone of forest that grades into a coastal strip of desert vegetation with some endemic species of prickly pear cactus (Opuntia). Fourteen species of finch are found on the islands. The evolutionary relationships amongst them have been traced by molecular techniques using microsatellite DNA that have confirmed the long‐held view that the family tree of the Galápagos finches radiated from a single trunk: a single ancestral species that invaded the islands from the mainland of Central America. The molecular data also provide strong evidence that the warbler finch (Certhidea olivacea) was the first to split off from the founding group and is likely to be the most similar to the original colonist ancestors. The entire process of evolutionary divergence of these species appears to have happened in less than 3 million years.

Figure 1.9 Many different species of Darwin’s finches have evolved on the Galápagos Islands. (a) Map of the Galápagos Islands showing their position relative to Central America; on the equator 5° equals approximately 560 km. (b) A reconstruction of the evolutionary history of the Galápagos finches based on variation in the length of microsatellite DNA. (A microsatellite is a tract of repetitive DNA in which certain DNA motifs, ranging in length from 2 to 5 base pairs, are repeated, with the number of repeats varying in alleles of individuals.) A measure of the genetic difference between species is shown by the length of the horizontal lines. The feeding habits of the various species are also shown. Drawings of the birds’ heads are proportional to actual body size. The maximum amount of black colouring in male plumage and the average body mass are shown for each species. C, Camarhynchus; Ce, Certhidea; G, Geospiza; P, Platyspiza; Pi, Pinaroloxias. (c) Gene flow for the four species on Daphne Major, through interbreeding with other species on the island and with immigrants of the same and other species from the nearby islands. Flow is measured as the effective number of individuals per generation. For genes to flow, the first‐generation hybrid offspring must themselves mate with one of the parental species. Genes flow from G. fortis to G. scandens when the hybrid sings the G. scandens song (because its father did) and vice versa for genes flowing from G. scandens to G. fortis. The population of G. fulginosa on Daphne Major is very small, and hence the flow of genes into G. fortis comes from immigrants from other islands.

Source: (b) After Petren et al. (1999). (c) After Grant & Grant (2010).

Isolation – both of the archipelago itself and of individual islands within it – has led to an original evolutionary line radiating into a series of species, each matching its own environment. Populations of ancestor species became reproductively isolated, most likely after chance colonisation of different islands within the archipelago, and evolved separately for a time. Secondary contact phases subsequently occurred as a result of movements between islands that brought non‐hybridising biospecies together that then evolved to fill different niches that elsewhere in the world are filled by quite unrelated species. Members of one group, including Geospiza fuliginosa and G. fortis, have strong bills and hop and scratch for seeds on the ground. G. scandens has a narrower and slightly longer bill and feeds on the flowers and pulp of the prickly pears as well as on seeds. Finches of a third group have parrot‐like bills and feed on leaves, buds, flowers and fruits, and a fourth group with a parrot‐like bill (Camarhynchus psittacula) has become insectivorous, feeding on beetles and other insects in the canopy of trees. A so‐called woodpecker finch, Camarhynchus (Cactospiza) pallida, extracts insects from crevices by holding a spine or a twig in its bill, while yet a further group includes the warbler finch, which flits around actively and collects small insects in the forest canopy and in the air.

However, the biospecies compartments are not water‐tight. A study of the four species on the small island of Daphne Major, and of their possible interbreeding with birds from larger nearby islands, again using molecular techniques, is summarised in Figure 1.9c. The two most abundant species, Geospiza fortis and G. scandens, were subject to a greater flow of genes between one another than they were to genes from immigrants of their own species from other islands. Indeed, in the case of G. fortis, there was also a substantial flow of genes from G. fuliginosa immigrants from other islands. Thus, the ‘ideal’ of gene flow within a species but not between them is not borne out by the data. But the fact that there are ‘grey areas’ partway through the process does not diminish the importance of either the process of speciation or the concept of biospecies.

ring species – perfect examples of speciation in action, but why so rare?

That speciation is a process rather than an event is beautifully illustrated by the existence of ring species. In these, races or subspecies of a species that fall short of being full species themselves (i.e. distinct forms that are nonetheless capable of producing fertile hybrids) are arranged along a geographic gradient in such a way that the two ends of the gradient themselves meet, hence forming a ring, and where they do, they behave as good species despite being linked, back around the ring, by the series of interbreeding races. Thus, what would normally be a temporal sequence of events, that we can only presume to have happened, becomes frozen in space. That the phenomenon is theoretically feasible has been demonstrated using mathematical models (e.g. de Brito Martins & de Aguiar, 2016). But actual examples are rare, and several that have been proposed in the past have been called into question by modern molecular studies, leading Pereira and Wake (2015) to wonder whether ring species are an unfulfilled promise or, worse still, wish‐fulfilment fantasy.

The classic example is the extraordinary case of two species of sea gull. The lesser black‐backed gull (Larus fuscus) originated in Siberia and colonised progressively to the west, forming a chain or cline of different forms, spreading from Siberia to Britain and Iceland. The neighbouring forms along the cline are distinctive, but were assumed to hybridise readily in nature. Neighbouring populations are regarded as part of the same species and taxonomists give them only ‘subspecific’ status (e.g. L. fuscus graellsii, L. fuscus fuscus). Populations of the gull have, however, also spread east from Siberia, again forming a cline of freely hybridising forms. Together, the populations spreading east and west encircle the northern hemisphere. They meet and overlap in northern Europe. There, the eastward and westward clines have diverged so far that it is easy to tell them apart, and they are recognised as two different species, the lesser black‐backed gull (L. fuscus) and the herring gull (L. argentatus). Moreover, the two species do not hybridise: they have become true biospecies. In this remarkable example, then, we can see how two distinct species seem to have evolved from one primal stock, and that the stages of their divergence remain frozen in the cline that connects them.

However, modern molecular techniques to determine genetic relationships have revealed a more complex picture. Thus, while ancestral populations expanded in a roughly circular fashion, there have been intermittent periods of allopatric fragmentation and subsequent range expansion, leading to areas of secondary contact where hybridisation currently occurs. Population divergence, therefore, proceeded at least partly in allopatry, not exclusively through isolation by distance throughout a contiguous range, as the ring species concept requires. Moreover, adjacent subspecies have been found not necessarily to be each other’s closest relatives and evidence is lacking of closure of the circumpolar ring by colonisation of Europe by North American herring gulls, a cornerstone of the ring species concept (Martens & Packert, 2007).

A more convincing example involves bulbuls in the genus Alophoixus in montane habitats of the Indo‐Malayan bioregion. Fuchs et al. (2015) have shown that diversification is consistent with most criteria expected for ring species (Figure 1.10a). First, molecular analysis shows that the seven taxa (Figure 1.10b) are all descendants of a single ancestral species, and probably derive from a single colonisation from Sundaland. Second, neighbouring taxa are most closely related, suggesting that taxa have diverged from a stepping stone colonisation of the high‐elevation forest around Thailand’s lowlands (lowland ‘barriers’ A and B in Figure 1.10a). The current distribution suggests that divergence can be explained by isolation by distance, as assumed by the ring species concept (but also, partly, by periods of geographic isolation that probably occurred during climatic cycles following initial diversification of the complex). Third, gene flow between neighbouring taxa suggests that divergence and secondary contact between taxa around the ring have resulted in genetic intergradation. And fourth, demographic analyses indicate a recent expansion and geographic overlap of the oldest taxon (1) and its most distant relative (7), leading to closure of the ring. However, hybrids sampled at the terminus of the ring (where taxon 1 meets taxon 7) indicate that divergence has not been sufficient for complete reproductive isolation to evolve.

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.