independent (individualistic) responses by components of the biota to climatic change (115).
If continental speciation is promoted by temporarily insular conditions the demography and genetics of founding populations may be of importance. It frequently has been suggested that on small islands or in fragmented habitats major genetic changes can take place in the early history of the founding of a new population by a few individuals, or during the bottlenecks caused by subsequent population crashes (116–119). The changes are believed to involve a few major genes that comprise a strongly epistatic polygenic system. Certainly changes can be rapid under these demographic circumstances. Selection is likely to be effective during the period of rapid growth from low population numbers, particularly for low-frequency alleles (120). High speciation rates (77), a greater genetic gap between similar species than between the most different conspecific populations (76), and the fact that populations are large yet genetic differences are small (74, 79), have all been interpreted as evidence for founder effects arising in subdivided populations and contributing to bird speciation.
The theory of founder speciation was developed when speciation was viewed as the evolution of postmating isolation largely, if not entirely, in geographical isolation (116). Derivatives of it are useful to account for some speciation phenomena in Drosophila (118–121) and similar organisms, but for birds it needs to be reappraised in light of a refocus on the origin of premating isolation (7). The idea that closely related species of birds differ in coadapted syndromes of mating behavior with an extensive genetic basis (122) is not supported by modern studies of hybridization and imprinting. The theory of founder effects does not explain how novel features like plumage traits arise. Founder effects may have contributed to bird speciation in the more limited way of altering the frequencies of alleles already in existence at the time of founding of a new population and initiating the evolution of premating isolating mechanisms.
The process of speciation is completed with the cessation of genetic exchange. In broad outline the last stages of speciation are known, but the genetic basis to the physiological details of postmating isolation are not. As species diverge they accumulate different mutations that contribute to lowered viability and fertility of hybrids, possibly also to prezygotic incompatibilities in the female reproductive tract. For example, hybrids of Agapornis parrots develop excessive fat, lipomas, defeathering (males), and gout (uric acid crystals in joints), and females are sterile (69). In accordance with Haldane’s rule, genetic problems first arise in the heterogametic females (123, 124). Premating isolation increases as these forms of postzygotic isolation develop. The sexual display activity and vocalizations of hybrids becomes reduced (e.g., see refs. 64 and 69) or disrupted at points in a courtship sequence corresponding to differences between the parental species (69, 125). The disruptions are caused by conflicts between incompatible units of behavior, missing parts of the repertoire of one or both parental species, or unusual behaviors not expressed by either parental species. Sexual behavior breaks down altogether and is not exhibited in hybrids produced in captivity between very disparate parental species, and cannot be induced by a large dose of sex hormones (67). Such species do not interbreed in nature.
Genetic incompatibilities that conform to Haldane’s rule do not always arise in the simple speciation process of one species splitting into two. Sometimes they arise between two species so formed only after each of them has split farther into yet more species. The frequency of this is unknown.
As a means of summarizing the preceding discussion and survey of the literature we suggest there are six rules of speciation in birds:
Speciation is initiated in allopatry.
The sympatric phase of the speciation process is established after an allopatric period of ecological divergence.
Allopatric evolution of premating isolating mechanisms precedes the evolution of postmating mechanisms in allopatry or sympatry.
Premating mechanisms are governed mainly by additive effects of polygenes, postmating mechanisms are due mainly to nonadditive genetic effects (dominance and epistasis).
Premating mechanisms include effects of the cultural process of sexual imprinting.
Postzygotic incompatibilities arise first in females. This is Haldane’s rule applied to birds in which females are the heterogametic sex.
All rules have exceptions, otherwise they would be laws, and it is doubtful if there are any speciation laws. Birds provide overwhelming support for Haldane’s rule (126), with a few exceptions affecting fertility (e.g., see refs. 32 and 65) but apparently none affecting viability in captive birds (ref. 32; but see ref. 127). Rule 5 would seem to have the greatest number of exceptions, particularly among those species lacking paternal care (128). We include it on the strength of a literature survey that concluded that sexual imprinting “seems to have been found wherever it has been looked for, and should be considered the rule rather than exceptional for the development of mate preferences in birds” (53). The rules should apply to other nonavian taxa, to varying degrees.
We conclude with a caveat. Almost 10,000 bird species are recognized under the biological species concept (129). Interpretations of speciation have been applied to perhaps 500 of them. The genetic basis of variation in premating isolating traits believed to be involved in speciation is known (incompletely) for less than 100 species, and the genetic basis of postmating isolation is virtually unknown for all of them. The knowledge base from which to generalize about the genetics of bird speciation is precariously thin. Recognition of this should be a stimulus for future research. The ease with which closely related species can be induced to hybridize in captivity suggests that a program of experimental hybridization has much to teach us about the genetics of bird speciation.
We are grateful to the A. von Humboldt Foundation and Peter Berthold of the Max-Planck-Institut at Radolfzell for support while this paper was written, and to T.D.Price, D.S.Woodruff, and an anonymous referee for helpful comments. Research on Darwin’s finches has been supported by the National Science and Engineering Research Council (Canada) and the National Science Foundation (USA).
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