Abstract

Studies of ecological speciation are often biased towards extrinsic sources of selection against hybrids, resulting from intermediate hybrid morphology, but the knowledge of how genetic incompatibilities accumulate over time under natural conditions is limited. Here we focus on a physiological trait, metabolic rate, which is central to life history strategies and thermoregulation but is also likely to be sensitive to mismatched mitonuclear interactions. We measured the resting metabolic rate of male collared, and pied flycatchers as well as of naturally occurring F1 hybrid males, in a recent hybrid zone. We found that hybrid males had a higher rather than intermediate metabolic rate, which is indicative of hybrid physiological dysfunction. Fitness costs associated with elevated metabolic rate are typically environmentally dependent and exaggerated under harsh conditions. By focusing on male hybrid dysfunction in an eco-physiological trait, our results contribute to the general understanding of how combined extrinsic and intrinsic sources of hybrid dysfunction build up under natural conditions.

Highlights

  • Ecological speciation, where barriers to gene flow are the result of divergent adaptation to environmental conditions, is thought to be a common mechanism by which new species form [1,2,3]

  • Hybrid dysfunction caused by interacting genes that have diverged in different populations [7, 8] can be the result of random genetic drift, coevolution resulting from genetic conflict or divergent natural and sexual selection [9, 10]

  • We report elevated metabolic rate of male F1 hybrids resulting from both types of pairing combinations between pied and collared flycatchers

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Summary

Introduction

Ecological speciation, where barriers to gene flow are the result of divergent adaptation to environmental conditions, is thought to be a common mechanism by which new species form [1,2,3]. Empirical studies on ecological speciation have generally been focused on young radiations and a subset of sources of reproductive isolation, which typically do not include genetic incompatibilities affecting hybrid viability or fertility [1, 2, 4]. Such incompatibilities are likely to evolve slowly and accumulate over time [5, 6], but whether and how ecological divergence leads to a gradual build up of genetic differences that cause combined effects of environmental and physiological mismatches in hybrids remains largely unexplored. Evidence for Dobzhansky-Muller (DM) interactions causing hybrid lethality or sterility have been

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