Abstract

All organisms depend on input of exogenous compounds that cannot be internally produced. Gain and loss of such dependencies structure ecological communities and drive species’ evolution, yet the evolution of mechanisms that accommodate these variable dependencies remain elusive. Here, we show that historical cycles of gains and losses of external dependencies in avian carotenoid-producing networks are linked to their evolutionary diversification. This occurs because internalization of metabolic controls—produced when gains in redundancy of dietary inputs coincide with increased branching of their derived products—enables rapid and sustainable exploration of an existing network by shielding it from environmental fluctuations in inputs. Correspondingly, loss of internal controls constrains evolution to the rate of the gains and losses of dietary precursors. Because internalization of a network’s controls necessarily bridges diet-specific enzymatic modules within a network, it structurally links local adaptation and continuous evolution even for traits fully dependent on contingent external inputs.

Highlights

  • All organisms depend on input of exogenous compounds that cannot be internally produced

  • The profiles were dominated by sources, as expected for traits dependent on dietary inputs, we observed a surprising extent of internal control in networks of many lineages (Fig. 2b)

  • ER randomization revealed that real avian carotenoid networks required more controls than a randomized network of the same size and complexity (Supplementary Fig. 2) and identified three key features of real carotenoid networks—(1) redundancy in source controls was associated with accumulation of metabolic expansions that required internal controls, (2) sink controls were rare, and (3) networks were dominated by only one control type at any given time

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Summary

Introduction

All organisms depend on input of exogenous compounds that cannot be internally produced. We show that historical cycles of gains and losses of external dependencies in avian carotenoid-producing networks are linked to their evolutionary diversification. Because internalization of a network’s controls necessarily bridges diet-specific enzymatic modules within a network, it structurally links local adaptation and continuous evolution even for traits fully dependent on contingent external inputs. 1234567890():,; Evolution proceeds by forming continuous lineages from past functional solutions of ancestors to the features of extant forms In this historical process, as species evolve adaptations and form associations with other species, they inevitably gain and lose their dependence on inputs from the external environments and other species[1,2,3]. To the extent that these properties reflect a network’s current function, the propensity of a node to control the network can be gained or lost, thereby providing a mechanistic link between a current adaptation and evolutionary change[21]

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