Abstract
BackgroundThe origin of complex adaptations is one of the most controversial questions in biology. Environmental induction of novel phenotypes, where phenotypic retention of adaptive developmental variation is enabled by organismal complexity and homeostasis, can be a starting point in the evolution of some adaptations, but empirical examples are rare. Comparisons of populations that differ in historical recurrence of environmental induction can offer insight into its evolutionary significance, and recent colonization of North America by the house finch (Carpodacus mexicanus) provides such an opportunity.ResultsIn both native (southern Arizona) and newly established (northern Montana, 18 generations) populations, breeding female finches exhibit the same complex adaptation – a sex-bias in ovulation sequence – in response to population-specific environmental stimulus of differing recurrence. We document that, in the new population, the adaptation is induced by a novel environment during females' first breeding and is subsequently retained across breeding attempts. In the native population, first-breeding females expressed a precise adaptive response to a recurrent environmental stimulus without environmental induction. We document strong selection on environmental cue recognition in both populations and find that rearrangement of the same proximate mechanism – clustering of oocytes that become males and females – can enable an adaptive response to distinct environmental stimuli.ConclusionThe results show that developmental plasticity induced by novel environmental conditions confers significant fitness advantages to both maternal and offspring generations and might play an important role not only in the successful establishment of this invasive species across the widest ecological range of extant birds, but also can link environmental induction and genetic inheritance in the evolution of novel adaptations.
Highlights
The origin of complex adaptations is one of the most controversial questions in biology
When individuals vary in their response to the novel stimulus, when this variability is heritable, and the stimulus is recurrent, such environmental induction can lead to eventual genetic determination of a novel adaptation [7,8]
Response to environmental stimulus Sex-bias in ovulation sequence of first-breeding females was closely associated with the number of critical temperature days during oogenesis in Montana (MT hereafter; maximum likelihood estimation F2 = 45.28, p < 0.001) and with number of mites at the nest site in Arizona (AZ hereafter; F2 = 106.3, p < 0.001), but the shape of the relationship differed between the populations
Summary
The origin of complex adaptations is one of the most controversial questions in biology. Environmental induction of novel phenotypes, where phenotypic retention of adaptive developmental variation is enabled by organismal complexity and homeostasis, can be a starting point in the evolution of some adaptations, but empirical examples are rare. Evolutionary biology is concerned with explaining the origin and diversification of organismal forms. The central thesis of this view is that evolutionary novelty often involves reorganization of preexisting phenotypes [9,10] and this results in similarity of the novel changes among individuals, facilitates response to novel selection pressures, and can lead to genetic assimilation of the novel trait [9,11,12,13,14,15,16]. Empirical documentation of evolutionary persistence of environmentally induced adaptations is rare in natural populations [17,18,19]
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