One of the best ways of showing evolutionary continuity between species and geographic races is to demonstrate that hybridization still occurs between closely related species. In Victorian times and early this century, naturalists were very interested, like "stamp-collectors", in freaks of nature, including rare hybrids between species. Between the 1930s and about 1980, there was decreased interest about the peculiarities of nature, and increased emphasis on the "fundamental" biological "realities" of animal species. (Hybridization between plant species is so abundant and easily shown, of course, that this rather myopic view of "pure", "good" species has never really caught on among botanists). Widely used field guides from this period often omit pictures even of common hybrids of birds and butterflies that can be seen in the wild, while treating much rarer or even extinct species in the same book. Recently, however, there has been renewed interest in all aspects of biodiversity, including that within species, and it is possible to discern a return of interest in variants, hybrids, and exceptions ("bad species") as well as the good species. In some beautiful recent books, often thorough world treatments of particular groups of butterflies and birds, hybridization between species is again becoming well-documented.
There has also been an impressive amount of recent work on hybrid zones, but most of this work has concentrated, perhaps for obvious reasons, on zones where hybrids are easily obtained, such as the hybrid zone between races of Heliconius melpomene in Eastern Ecuador (see also Henry Walter Bates' (1863) pioneering work on natural hybridization in Heliconius, and William Beebe's (1955) first experimental crosses; these are now considered to be hybridization between geographic races of the same species). Arguably, these studies contribute little to understanding speciation (JM criticises himself here ... and hybrid zone studies are interesting for other reasons!), because the forms that interact have clearly not speciated.
Hybrids between species are much rarer: usually less than one in a thousand individuals in a pair of hybridizing species are recognizable hybrids, and often even fewer. What is not generally realized, however, is that the fraction of all species that hybridize is high (Mallet 2005). A world-wide survey of birds has shown that around 9% of species hybridize (Panov in Grant & Grant 1992), and in European butterflies including Hesperiidae, the rate is about 12% of species (Guillaumin & Descimon 1976) - here species are classified conservatively using the polytypic species concept, not the so-called "phylogenetic concept", so hybridization between geographic forms is not considered as interspecific hybridization, unless hybrids are very rare in the zone of overlap. Some genera and higher groups have much higher rates, over 20% of species, for example in the American warblers, the birds of paradise, and Darwin's finches among the birds (Grant & Grant 1992). See also Mallet (2005) for a review of natural hybridization in animals which surveys a number of groups, including birds, mammals, as well as insects, and compares them to hybridization rates in plants.
A somewhat related topic is the topic of hybrid speciation. The speciation of taxa due to hybridization requires, of course, the existence of ongoing natural hybridization documented here. Recent publications provide conclusive evidence that at least one of the Heliconiina, Heliconius heurippa, is a hybrid species, having characteristics inherited from the local races of both Heliconius cydno and H. melpomene (Salazar et al. 2005, Mavárez et al. 2006).
We here provide an updated database of wild-caught interspecific Heliconius hybrids. In this butterfly genus, about 26% of species are known to hybridize (Mallet et al. 1998, Mallet 2005).
For many of these species, laboratory hybrids have now been produced. We have excluded any laboratory hybrids from the database because we were interested here mainly in the potential for natural hybrids. However, the artificially produced hybrids are a useful confirmation of the hybrid status of the wild-caught individuals. Several recent studies have dealt with laboratory hybridization, the inheritance of colour pattern, and hybrid viability and sterility between Heliconius species (Jiggins & McMillan 1997, McMillan et al. 1997, Naisbit et. al. 2002, 2003). Gynandromorphs, presumably a result of chimaeric development of separately fertilized zygotes, are relatively common in hybridization experiments between geographic races of Heliconius species. This may merely be due to the greater ease of detection of gynandromorphs in populations polymorphic for major colour pattern differences. Larry Gilbert (pers. comm.) obtained an interesting gyndandromorph Heliconius cydno x H. melpomene hybrid, perhaps the only one of its kind.
Several specimens are unique and may be simple mutational variants, as opposed to hybrids. These have been excluded from our database as far as possible; for example, we here show a very odd Eueides caught in the wild, and an aberrant Heliconius charithonia produced in an insectary. Other probable mutant specimens are shown here.
Between most pairs of species, hybrids are very rare in nature. The only exceptions are H. himera and H. erato, which hybridize wherever their ranges abut in contact zones. In this pair of species, there is no inviability or sterility among the hybrids, backcrosses, or F2 (McMillan et al. 1997). The species remain distinct because of mate choice (which is about 5% "leaky"), and strong ecological selection against hybrids.
In another good example, Heliconius melpomene and H. cydno hybridize regularly (though at low frequency, maybe 1/1000 individuals are hybrids) throughout their joint range, and their distributions overlap extensively throughout W. Ecuador, Andean Colombia and Venezuela, and Central America. Here female hybrids have been found in the laboratory to be sterile (Naisbit et. al. 2002, 2003), but wild hybrids are often backcross phenotypes, showing that males backcross in the wild as well as in captivity. Once hybrids have been produced in a local population, backcross phenotypes may survive at high frequency for several generations. In a collection of 103 H. cydno and H. melpomene made by Jesús Mavárez in the botanic garden of San Cristobal, Táchira, Venezuela, seven were putative backcross hybrids, even though such hybrids are rare elsewhere. These two species are extremely closely related genetically, and the rarity of hybrids is due to very strong mate discrimination (Jiggins et al. 2001). Some mtDNA studies put H. cydno within the genealogy of H. melpomene; i.e. H. cydno is little more than a clade of Heliconius melpomene that has speciated,suggesting H. melpomene a paraphyletic remnant (Brower 1996).
An important conclusion that can be drawn from this kind of data is that speciation doesn't suddenly lead to a complete absence of gene flow. There may be several millions of years after speciation during which genes may be exchanged between newly-evolved, recognizably and ecologically distinct species. Given that new species are able to maintain genetic differences in spite of hybridization, interspecific gene flow between animal species could be quite common, and may even contribute to heritability and genetic variation within animal species, as has been shown for the Darwin's finches by Grant & Grant (1992). There is very clear evidence in the specimens we illustrate that wild hybrids between H. melpomene and H. cydno, and between H. erato and H. himera, backcross regularly. We are currently undertaking studies to investigate whether significant gene flow occurs in some parts of the genome between Heliconius melpomene and H. cydno, while leaving other parts of the genome, affecting ecological and colour pattern differences, intact.
Another conclusion is that reinforcement (adaptive evolution of mate choice) may be more likely than previously realized. Reinforcement is often seen as unlikely because the evolution of mating isolation has to race against the breakdown of the genetic differences due to hybridization - the latter will usually win. But, given that newly emerged species can stably maintain their genetic differences in the face of gene flow, further mate choice should be able to evolve adaptively to prevent the production of genetically inferior hybrids.
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