Abstract
Robustness against environmental fluctuations within an adaptive state should preclude exploration of new adaptive states when the environment changes. Here, we study transitions between adaptive associations of feather structure and carotenoid uptake to understand how robustness and evolvability can be reconciled. We show that feather modifications induced by unfamiliar carotenoids during a range expansion are repeatedly converted into precise coadaptations of feather development and carotenoid accommodation as populations persist in a region. We find that this conversion is underlain by a uniform and coordinated increase in the sensitivity of feather development to local carotenoid uptake, indicative of cooption and modification of the homeostatic mechanism that buffers feather growth in the evolution of new adaptations. Stress-buffering mechanisms are well placed to alternate between robustness and evolvability and we suggest that this is particularly evident in adaptations that require close integration between widely fluctuating external inputs and intricate internal structures.
Highlights
Robustness against environmental fluctuations within an adaptive state should preclude exploration of new adaptive states when the environment changes
It is difficult to infer the historical role of stress-buffering mechanisms from comparisons of contemporary adaptations alone, because homeostatic systems necessarily suppress variation that interferes with current functioning and new adaptations subsume preceding adaptations in evolution[13]
It has been known that the uptake of carotenoids into barbs often interferes with barbule development, underpinning a textbook explanation for why feathers that are structurally specialized, such as flight and down feathers, are buffered against significant carotenoid uptake and are rarely colorful[27]
Summary
Robustness against environmental fluctuations within an adaptive state should preclude exploration of new adaptive states when the environment changes. It is not known whether the feather modifications resulting from uptake of external carotenoids are adaptations to maximize coloration (Fig. 2b), transient malformations that require subsequent evolution of greater buffering of feather growth (Fig. 2c), or evidence of evolved plasticity, where local carotenoids directly induce feather growth modification[29,30] (Fig. 2d) We test these scenarios using the recent colonization of western North America by house finches (Haemorhous mexicanus), which has produced replicated, hierarchical sequences of known-age populations across one of the widest ecological ranges of any extant bird species31(Fig. 3).
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