Ladies and gentes: maternally inherited DNA and ancient honeyguide host races.

A vian interspecific brood parasitism occurs when a female bird uses a different host species to incubate and rear her offspring. Studies of this parasitic behavior have provided some of nature’s most compelling examples of coevolutionary interactions (1). Avian brood parasites exhibit wide variation in host specificity, ranging from one or a few hosts to hundreds, and there is a concomitant degree of coevolution of traits between parasite and host. For example, within many species of cuckoos, and some species of cowbirds, parasite eggs visually and morphologically match those of their hosts. If there is variation in egg characteristics among different host species, and selection promotes egg matching to avoid host recognition and rejection of parasitic eggs, this can lead to the evolution of host-specific races of parasites (called gentes). The evolution of gentes within species was considered problematic until it was determined that, unlike mammals, female birds have heterogametic sex chromosomes (i.e., females have 1 Z chromosome and 1 W chromosome, whereas males have 2 Z chromosomes). Thus, the genes that determine egg morphology and host nest selection behavior might reside on the female-specific W chromosome and not be available to recombine with genetic material from males (2). However, not until the recent advent of molecular tools has there been evidence for the role of female control of host egg matching or for the time frame of host-race evolution. Thus far, research has revealed somewhat conflicting evidence for direct female control of egg and nestling traits, and it has suggested very recent (<100 kya) host-race divergences in cuckoos and cowbirds (3– 5). Now, however, using an mtDNA analog for the W chromosome, a study in PNAS by Spottiswoode et al. (6) on the brood parasitic greater honeyguide describes an unexpected ancient divergence among gentes and greatly expands our understanding of how such host races can evolve. Among the 100 species of obligate brood parasites (about 1% of the roughly 10,000 described avian species) are the more familiar cuckoos and cowbirds, but less common examples include African viduid finches, a South American duck, and the relatively unstudied honeyguides (1). The honeyguides (Indicatoridae) consist of 17 species in four genera, with most species occurring in Africa and 2 species that leak out into southern Asia. Although drab and unremarkable in plumage, honeyguides are among the most interesting of birds because of two unusual features of their life history and associated behaviors (7). First, as their name implies, some honeyguide species are known to recruit and guide a select group of mammals, including humans (Homo sapiens), and perhaps ratels (Mellivora capensis), to beehives. The mammal will break open the hive, enabling it to retrieve the honey, leaving the honeyguide with a meal of wax and bee larvae (but apparently not the honey) from the honeycomb. Honeyguides are one of a few types of birds that practice cerophagy (wax eating). They have been suggested to use specialized enzymes and/or bacterial gut symbionts to assist in wax digestion (7, 8), but this has not been confirmed with recent experimental work (9). Second, all honeyguides are obligate brood parasites, laying their eggs in the nests of a range of bird species, mostly those nesting in cavities. Female honeyguides will usually puncture a host egg before parasitizing the host nest with their own single white egg. They have another unusual adaptation for ensuring success of their young: Unlike many cuckoo nestlings, which will eject a host egg or nestling from the nest, honeyguide nestlings have a very sharp bill hook that they use to lacerate and kill host nestlings in the nest (7, 10). The “murderous” hook is present in very young chicks and is lost during development of the bill after about 2 wk of age. Spottiswoode et al. (6) document that individual greater honeyguides that parasitize different host species show significant differences in egg size or shape that tend to match the size and shape of eggs of their hosts. However, unlike many other brood parasites, greater honeyguides do Fig. 1. Shown is a schematic of the pattern of mtDNA sequence divergence in greater honeyguides that parasitize two types of hosts: those that nest in cavities in trees and those that nest in burrows in the ground [as described by Spottiswood et al. (6)]. MtDNA divergence indicates a surprisingly long time period since separation of female lineages, whereas similarity in nuclear genes suggests mating at random with respect to host nest type. Thus, selection of different host nest types and similarity in egg morphology are likely to be under female genetic control. Pictured are the greater honeyguide (Middle, Indicator indicator), little bee-eater (Top,Merops pusillus), and African hoopoe (Bottom, Upupa africana) (Top and Bottom, photographs courtesy of Mark Anderson; Middle, photograph courtesy of Warwick Tarboton.)