Conservation evo-devo: preserving biodiversity by understanding its origins

Unprecedented rates of species extinction increase the urgency for effective conservation biology management practices. Thus, any improvements in practice are vital and we suggest that conservation can be enhanced through recent advances in evolutionary biology, specifically advances put forward by evolutionary developmental biology (i.e., evo-devo). There are strong overlapping conceptual links between conservation and evo-devo whereby both fields focus on evolutionary potential. In particular, benefits to conservation can be derived from some of the main areas of evo-devo research, namely phenotypic plasticity, modularity and integration, and mechanistic investigations of the precise developmental and genetic processes that determine phenotypes. Using examples we outline how evo-devo can expand into conservation biology, an opportunity which holds great promise for advancing both fields

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

The genetic architecture underlying the evolution of a rare piscivorous life history form in brown trout after secondary contact and strong introgression

Identifying the genetic basis underlying phenotypic divergence and reproductive isolation is a longstanding problem in evolutionary biology. Genetic signals of adaptation and reproductive isolation are often confounded by a wide range of factors, such as variation in demographic history or genomic features. Brown trout ( ) in the Loch Maree catchment, Scotland, exhibit reproductively isolated divergent life history morphs, including a rare piscivorous (ferox) life history form displaying larger body size, greater longevity and delayed maturation compared to sympatric benthivorous brown trout. Using a dataset of 16,066 SNPs, we analyzed the evolutionary history and genetic architecture underlying this divergence. We found that ferox trout and benthivorous brown trout most likely evolved after recent secondary contact of two distinct glacial lineages, and identified 33 genomic outlier windows across the genome, of which several have most likely formed through selection. We further identified twelve candidate genes and biological pathways related to growth, development and immune response potentially underpinning the observed phenotypic differences. The identification of clear genomic signals divergent between life history phenotypes and potentially linked to reproductive isolation, through size assortative mating, as well as the identification of the underlying demographic history, highlights the power of genomic studies of young species pairs for understanding the factors shaping genetic differentiation

Parallel selection on ecologically relevant gene functions in the transcriptomes of highly diversifying salmonids

Background: Salmonid fishes are characterised by a very high level of variation in trophic, ecological, physiological, and life history adaptations. Some salmonid taxa show exceptional potential for fast, within-lake diversification into morphologically and ecologically distinct variants, often in parallel; these are the lake-resident charr and whitefish (several species in the genera Salvelinus and Coregonus). To identify selection on genes and gene categories associated with such predictable diversifications, we analysed 2702 orthogroups (4.82 Mbp total; average 4.77 genes/orthogroup; average 1783 bp/orthogroup). We did so in two charr and two whitefish species and compared to five other salmonid lineages, which do not evolve in such ecologically predictable ways, and one non-salmonid outgroup. Results: All selection analyses are based on Coregonus and Salvelinus compared to non-diversifying taxa. We found more orthogroups were affected by relaxed selection than intensified selection. Of those, 122 were under significant relaxed selection, with trends of an overrepresentation of serine family amino acid metabolism and transcriptional regulation, and significant enrichment of behaviour-associated gene functions. Seventy-eight orthogroups were under significant intensified selection and were enriched for signalling process and transcriptional regulation gene ontology terms and actin filament and lipid metabolism gene sets. Ninety-two orthogroups were under diversifying/positive selection. These were enriched for signal transduction, transmembrane transport, and pyruvate metabolism gene ontology terms and often contained genes involved in transcriptional regulation and development. Several orthogroups showed signs of multiple types of selection. For example, orthogroups under relaxed and diversifying selection contained genes such as ap1m2, involved in immunity and development, and slc6a8, playing an important role in muscle and brain creatine uptake. Orthogroups under intensified and diversifying selection were also found, such as genes syn3, with a role in neural processes, and ctsk, involved in bone remodelling. Conclusions: Our approach pinpointed relevant genomic targets by distinguishing among different kinds of selection. We found that relaxed, intensified, and diversifying selection affect orthogroups and gene functions of ecological relevance in salmonids. Because they were found consistently and robustly across charr and whitefish and not other salmonid lineages, we propose these genes have a potential role in the replicated ecological diversifications

RADseq and mate choice assays reveal unidirectional gene flow among three lamprey ecotypes despite weak assortative mating: Insights into the formation and stability of multiple ecotypes in sympatry

Adaptive divergence with gene flow often results in complex patterns of variation within taxa exhibiting substantial ecological differences among populations. One example where this may have occurred is the parallel evolution of freshwater‐resident nonparasitic lampreys from anadromous‐parasitic ancestors. Previous studies have focused on transitions between these two phenotypic extremes, but here, we considered more complex evolutionary scenarios where an intermediate freshwater form that remains parasitic is found sympatrically with the other two ecotypes. Using population genomic analysis (restriction‐associated DNA sequencing), we found that a freshwater‐parasitic ecotype was highly distinct from an anadromous‐parasitic form (Qlake‐P = 96.8%, Fst = 0.154), but that a freshwater‐nonparasitic form was almost completely admixed in Loch Lomond, Scotland. Demographic reconstructions indicated that both freshwater populations likely derived from a common freshwater ancestor. However, while the nonparasitic ecotype has experienced high levels of introgression from the anadromous‐parasitic ecotype (Qanad‐P = 37.7%), there is no evidence of introgression into the freshwater‐parasitic ecotype. Paradoxically, mate choice experiments predicted high potential for gene flow: Males from all ecotypes were stimulated to spawn with freshwater‐parasitic females, which released gametes in response to all ecotypes. Differentially fixed single nucleotide polymorphisms identified genes associated with growth and development, which could possibly influence the timing of metamorphosis, resulting in significant ecological differences between forms. This suggests that multiple lamprey ecotypes can persist in sympatry following shifts in adaptive peaks, due to environmental change during their repeated colonization of post‐glacial regions, followed by periods of extensive gene flow among such diverging populations

A phenotypically plastic magic trait promoting reproductive isolation in sticklebacks?

This study identifies one possible mechanism whereby gene flow is interrupted in populations undergoing evolutionary divergence in sympatry; this is an important issue in evolutionary biology that remains poorly understood. Variation in trophic morphology was induced in three-spined stickleback by exposing them from an early age either to large benthic or to small pelagic prey. At sexual maturity, females given a choice between two breeding males, showed positive assortative mate choice for males raised on the same diet as themselves. The data indicate that this was mediated through a preference for males with trophic morphology similar to that of fish with which the females were familiar (from their pre-testing holding tanks). In trials where the female did not choose the most familiar male, the evidence suggests that either she had difficulty discriminating between two similar males or was positively choosing males with more extreme morphologies (more benthic-like or pelagic-like). This study has shown for the first time that expression of a plastic trait induced at an early age, not only results in specialisation for local foraging regimes but can also play a significant role in mate choice. This is equivalent to an environmentally induced, plastic version of the “magic traits” that promote ecologically-driven divergence in sympatry, hence the proposed descriptor “plastic magic trait”

Patterns and repeatability of multi-ecotype assemblages of sympatric salmonids

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Genomic underpinnings of head and body shape in Arctic charr ecomorph pairs

Across its Holarctic range, Arctic charr (Salvelinus alpinus) populations have diverged into distinct trophic specialists across independent replicate lakes. The major aspect of divergence between ecomorphs is in head shape and body shape, which are ecomorphological traits reflecting niche use. However, whether the genomic underpinnings of these parallel divergences are consistent across replicates was unknown but key for resolving the substrate of parallel evolution. We investigated the genomic basis of head shape and body shape morphology across four benthivore–planktivore ecomorph pairs of Arctic charr in Scotland. Through genome-wide association analyses, we found genomic regions associated with head shape (89 SNPs) or body shape (180 SNPs) separately and 50 of these SNPs were strongly associated with both body and head shape morphology. For each trait separately, only a small number of SNPs were shared across all ecomorph pairs (3 SNPs for head shape and 10 SNPs for body shape). Signs of selection on the associated genomic regions varied across pairs, consistent with evolutionary demography differing considerably across lakes. Using a comprehensive database of salmonid QTLs newly augmented and mapped to a charr genome, we found several of the head- and body-shape-associated SNPs were within or near morphology QTLs from other salmonid species, reflecting a shared genetic basis for these phenotypes across species. Overall, our results demonstrate how parallel ecotype divergences can have both population-specific and deeply shared genomic underpinnings across replicates, influenced by differences in their environments and demographic histories

Evolvability under climate change: bone development and shape plasticity are heritable and correspond with performance in Arctic charr (Salvelinus alpinus)

Environmental conditions can impact the development of phenotypes and in turn the performance of individuals. Climate change, therefore, provides a pressing need to extend our understanding of how temperature will influence phenotypic variation. To address this, we assessed the impact of increased temperatures on ecologically significant phenotypic traits in Arctic charr (Salvelinus alpinus). We raised Arctic charr at 5°C and 9°C to simulate a predicted climate change scenario and examined temperature-induced variation in ossification, bone metabolism, skeletal morphology, and escape response. Fish reared at 9°C exhibited less cartilage and bone development at the same developmental stage, but also higher bone metabolism in localized regions. The higher temperature treatment also resulted in significant differences in craniofacial morphology, changes in the degree of variation, and fewer vertebrae. Both temperature regime and vertebral number affected escape response performance, with higher temperature leading to decreased latency. These findings demonstrate that climate change has the potential to impact development through multiple routes with the potential for plasticity and the release of cryptic genetic variation to have strong impacts on function through ecological performance and survival