Several previous tests of this elegantly simple maternal inheritance hypothesis, first proposed by Reginald Punnett in 1933 ( 13, 14), have used mitochondrial DNA (mtDNA) to test whether parasitic females associated with different host species belong to distinct matrilines. When combined with environmentally determined host choice via imprinting ( 12), maternal genetic inheritance of egg mimicry would thus ensure that the egg phenotype of females is appropriate for the host species they parasitize. Alternatively, since female birds are heterogametic, maternal inheritance of egg mimicry genes via the W chromosome could ensure faithful transmission of adaptations from mother to daughter, even if females mate with males raised by different host species. First, females might mate only with males raised by the same host species, generating reproductive isolation and cryptic speciation between host-specialists ( 11). There are two potential solutions to this puzzle. The evolutionary puzzle of how such diversity in host-specific adaptations could evolve and be maintained within a single parasitic species was first recognized in 1910 ( 10). In some parasitic species that exploit multiple host species, phenotypically distinct host races (known as gentes in the context of avian brood parasitism) specialize on different host species by mimicking their respective egg phenotypes. Many hosts defend themselves by rejecting foreign eggs from their nests, which has led to the evolution of egg mimicry by parasites ( 8, 9). In this study, we demonstrate maternally inherited host-specific adaptation in a brood-parasitic bird and ask how a lack of sexual recombination shapes the coevolutionary arms race with its hosts.īrood parasites reproduce by laying eggs in the nests of other species, thereby exploiting the parental care behavior of their hosts.
This trade-off between the benefits and costs of uniparental inheritance may be especially acute when sex-linked loci control traits under reciprocal selection in dynamic arms races between antagonists. However, eliminating recombination can limit the adaptive potential of Y and W chromosomes and weaken the efficacy of selection ( 5). This uniparental and effectively asexual inheritance can protect coadapted genes from disruptive recombination, thereby ensuring faithful transmission of adaptation across generations ( 5– 7). However, this benefit can be lost when genes advantageous to the heterogametic sex arise on or relocate to the minor sex chromosome (e.g., W in birds or Y in mammals), the single copy of which is transmitted largely without recombination. Genetic recombination and heterozygosity generate evolutionary novelty ( 1, 2) and, therefore, promote adaptation in rapidly changing selective environments, an advantage considered pivotal to the evolution of sex. This illustrates an important cost of coding coevolved adaptations on the nonrecombining sex chromosome, which may impede further coevolutionary change by effectively reversing the advantages of sexual reproduction in antagonistic coevolution proposed by the Red Queen hypothesis.
The inability to generate novel genetic combinations likely prevents cuckoo finches from mimicking certain host phenotypes that are currently favored by selection (e.g., the olive-green colored eggs laid by some tawny-flanked prinia, Prinia subflava, females). However, maternal inheritance and the lack of sexual recombination likely disadvantage cuckoo finches by stifling further adaptation in the ongoing arms races with their individual hosts, which we show have retained biparental inheritance of egg phenotypes. Thus, maternal inheritance has enabled the evolution and maintenance of nested levels of mimetic specialization in a single parasitic species.
We further show that maternal inheritance not only underpins the mimicry of different host species but also additional mimetic diversification that approximates the range of polymorphic egg “signatures” that have evolved within host species as an escalated defense against parasitism. We demonstrate that host-specific egg mimicry in the African cuckoo finch Anomalospiza imberbis is maternally inherited, confirming the validity of an almost century-old hypothesis. This process is typically enhanced by genetic recombination and heterozygosity, but these sources of evolutionary novelty may be secondarily lost when uniparental inheritance evolves to ensure the integrity of sex-linked adaptations. In coevolutionary arms races, interacting species impose selection on each other, generating reciprocal adaptations and counter adaptations.
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