Parallelism in eco-morphology and gene expression despite variable evolutionary and genomic backgrounds in a Holarctic fish.

Understanding the extent to which ecological divergence is repeatable is essential for predicting responses of biodiversity to environmental change. Here we test the predictability of evolution, from genotype to phenotype, by studying parallel evolution in a salmonid fish, Arctic charr (Salvelinus alpinus), across eleven replicate sympatric ecotype pairs (benthivorous-planktivorous and planktivorous-piscivorous) and two evolutionary lineages. We found considerable variability in eco-morphological divergence, with several traits related to foraging (eye diameter, pectoral fin length) being highly parallel even across lineages. This suggests repeated and predictable adaptation to environment. Consistent with ancestral genetic variation, hundreds of loci were associated with ecotype divergence within lineages of which eight were shared across lineages. This shared genetic variation was maintained despite variation in evolutionary histories, ranging from postglacial divergence in sympatry (ca. 10-15kya) to pre-glacial divergence (ca. 20-40kya) with postglacial secondary contact. Transcriptome-wide gene expression (44,102 genes) was highly parallel across replicates, involved biological processes characteristic of ecotype morphology and physiology, and revealed parallelism at the level of regulatory networks. This expression divergence was not only plastic but in part genetically controlled by parallel cis-eQTL. Lastly, we found that the magnitude of phenotypic divergence was largely correlated with the genetic differentiation and gene expression divergence. In contrast, the direction of phenotypic change was mostly determined by the interplay of adaptive genetic variation, gene expression, and ecosystem size. Ecosystem size further explained variation in putatively adaptive, ecotype-associated genomic patterns within and across lineages, highlighting the role of environmental variation and stochasticity in parallel evolution. Together, our findings demonstrate the parallel evolution of eco-morphology and gene expression within and across evolutionary lineages, which is controlled by the interplay of environmental stochasticity and evolutionary contingencies, largely overcoming variable evolutionary histories and genomic backgrounds.

The physiological costs of prey switching reinforce foraging specialization.

Sympatric speciation is thought to be strongly linked to resource specialization with alternative resource use acting as a fundamental agent driving divergence. However, sympatric speciation through niche expansion is dependent on foraging specialization being consistent over space and time. Standard metabolic rate is the minimal maintenance metabolic rate of an ectotherm in a post-absorptive and inactive state and can constitute a significant portion of an animal's energy budget; thus, standard metabolic rate and growth rate are two measures frequently used as an indication of the physiological performance of individuals. Physiological adaptations to a specific diet may increase the efficiency with which it is utilized, but may have an increased cost associated with switching diets, which may result in a reduced standard metabolic rate and growth rate. In this study, we use the diet specialization often seen in polymorphic Arctic charr (Salvelinus alpinus) populations to study the effects of different prey on standard metabolic rate and growth rate as well as the effects that early prey specialization may have on the ability to process other prey types efficiently. We found a significant effect of prey type on standard metabolic rate and growth rate. Furthermore, we found evidence of diet specialization with all fish maintaining a standard metabolic rate and growth rate lower than expected when fed on a diet different to which they were raised, possibly due to a maladaptation in digestion of alternative prey items. Our results show that early diet specialization may be reinforced by the elevated costs of prey switching, thus promoting the process of resource specialization during the incipient stages of sympatric divergence.

A way forward with eco evo devo: an extended theory of resource polymorphism with postglacial fishes as model systems.

A major goal of evolutionary science is to understand how biological diversity is generated and altered. Despite considerable advances, we still have limited insight into how phenotypic variation arises and is sorted by natural selection. Here we argue that an integrated view, which merges ecology, evolution and developmental biology (eco evo devo) on an equal footing, is needed to understand the multifaceted role of the environment in simultaneously determining the development of the phenotype and the nature of the selective environment, and how organisms in turn affect the environment through eco evo and eco devo feedbacks. To illustrate the usefulness of an integrated eco evo devo perspective, we connect it with the theory of resource polymorphism (i.e. the phenotypic and genetic diversification that occurs in response to variation in available resources). In so doing, we highlight fishes from recently glaciated freshwater systems as exceptionally well-suited model systems for testing predictions of an eco evo devo framework in studies of diversification. Studies on these fishes show that intraspecific diversity can evolve rapidly, and that this process is jointly facilitated by (i) the availability of diverse environments promoting divergent natural selection; (ii) dynamic developmental processes sensitive to environmental and genetic signals; and (iii) eco evo and eco devo feedbacks influencing the selective and developmental environments of the phenotype. We highlight empirical examples and present a conceptual model for the generation of resource polymorphism - emphasizing eco evo devo, and identify current gaps in knowledge.

Ecosystem size predicts eco-morphological variability in a postglacial diversification.

Identifying the processes by which new phenotypes and species emerge has been a long-standing effort in evolutionary biology. Young adaptive radiations provide a model to study patterns of morphological and ecological diversification in environmental context. Here, we use the recent radiation (ca. 12k years old) of the freshwater fish Arctic charr (Salvelinus alpinus) to identify abiotic and biotic environmental factors associated with adaptive morphological variation. Arctic charr are exceptionally diverse, and in postglacial lakes there is strong evidence of repeated parallel evolution of similar morphologies associated with foraging. We measured head depth (a trait reflecting general eco-morphology and foraging ecology) of 1,091 individuals across 30 lake populations to test whether fish morphological variation was associated with lake bathymetry and/or ecological parameters. Across populations, we found a significant relationship between the variation in head depth of the charr and abiotic environmental characteristics: positively with ecosystem size (i.e., lake volume, surface area, depth) and negatively with the amount of littoral zone. In addition, extremely robust-headed phenotypes tended to be associated with larger and deeper lakes. We identified no influence of co-existing biotic community on Arctic charr trophic morphology. This study evidences the role of the extrinsic environment as a facilitator of rapid eco-morphological diversification.