Incomplete reproductive isolation following host shift in brood parasitic indigobirds

Abstract

Behavioural and molecular studies suggest that brood parasitic indigobirds (Vidua spp.) rapidly diversified through a process of speciation by host shift. However, behavioural imprinting on host song, the key mechanism promoting speciation in this system, may also lead to hybridization and gene flow among established indigobird species when and if female indigobirds parasitize hosts already associated with other indigobird species. It is therefore not clear to what extent the low level of genetic differentiation among indigobird species is due to recent common ancestry versus ongoing gene flow. We tested for reproductive isolation among three indigobird species in Cameroon, one of which comprises two morphologically indistinguishable host races. Mimicry of host songs corresponded with plumage colour in 184 male indigobirds, suggesting that females rarely parasitize the host of another indigobird species. Paternity analyses, however, suggest that imperfect specificity in host and/or mate choice allows for continuing gene flow between recently formed host races of the Cameroon Indigobird Vidua camerunensis; while 63 pairs of close relatives were associated with the same host, two strongly supported father-son pairs included males mimicking the songs of the two different hosts of V. camerunensis. Thus, complete reproductive isolation is not necessarily an automatic consequence of host shifts, a result that suggests an important role for natural and/or sexual selection in indigobird speciation.

Underappreciated Consequences of Phenotypic Plasticity for Ecological Speciation

“…However, it is not always obvious that habitat or resource imprinting should directly affect mating preferences. In the Vidua indigobirds, there is an imprinting effect of host song, such that nest parasites raised by the same host species tend to mate assortatively owing to learned elements of their own songs and preferences [103,104]. In many phytophagous insects, mating occurs on or near the host plant [102,105], making plant choice a "magic trait" simultaneously effecting ecological and sexual differentiation [31].…”

Effects on Population Divergence of Within-Generational Learning About Prospective Mates

“…; Balakrishnan et al. ), we know of no case where learning has been shown to be a major factor leading to speciation.…”

“…Intriguingly, with a single exception involving the unusual brood parasitic indigo birds (Vidua spp. ), which imprint on their host (Payne et al 2000;Sorenson et al 2003;Balakrishnan et al 2009), we know of no case where learning has been shown to be a major factor leading to speciation.…”

ddRAD-seq phylogenetics based on nucleotide, indel, and presence–absence polymorphisms: Analyses of two avian genera with contrasting histories

“…7B) supports the hypothesis that gene flow 812 among Vidua species has increased the level of gene tree discor-813 dance in this genus, and that differences between the genera are 814 not due solely to different timescales for speciation. 815 Hybridization between Vidua species has been documented 816 , and is likely facilitated by mate choice 817 behaviors that are shaped by host imprinting (Payne et al, 2000), 818 sympatry between ancestral and incipient species, and imperfect 819 host fidelity by female parasites (Balakrishnan et al, 2009). An 820 additional factor that may contribute to discordance among loci 821 is the possibility that a given parasitic species derives from multi- (Fig.…”