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Ecological speciation is the process by which barriers to gene flow between populations evolve due to adaptive divergence via natural selection. A relatively unexplored area in ecological speciation is the role of gene expression. Gene expression may be associated with ecologically important phenotypes not evident from morphology and play a role during colonization of new environments. Here we review two potential roles of gene expression in ecological speciation: (1) its indirect role in facilitating population persistence and (2) its direct role in contributing to genetically based reproductive isolation. We find indirect evidence that gene expression facilitates population persistence, but direct tests are lacking. We also find clear examples of gene expression having effects on phenotypic traits and adaptive genetic divergence, but links to the evolution of reproductive isolation itself remain indirect. Gene expression during adaptive divergence seems to often involve complex genetic architectures controlled by gene networks, regulatory regions, and “eQTL hotspots.” Nonetheless, we review how approaches for isolating the functional mutations contributing to adaptive divergence are proving to be successful. The study of gene expression has promise for increasing our understanding ecological speciation, particularly when integrative approaches are applied.

The two primary ways that species respond to heterogeneous environments is through local adaptation and phenotypic plasticity. The American eel (Anguilla rostrata) presents a paradox; despite inhabiting drastically different environments [1], the species is panmictic [2, 3]. Spawning takes place only in the southern Sargasso Sea in the Atlantic Ocean [1]. Then, the planktonic larvae (leptocephali) disperse to rearing locations from Cuba to Greenland, and juveniles colonize either freshwater or brackish/saltwater habitats, where they spend 3-25 years before returning to the Sargasso Sea to spawn as a panmictic species. Depending on rearing habitat, individuals exhibit drastically different ecotypes [4-6]. In particular, individuals rearing in freshwater tend to grow slowly and mature older and are more likely to be female in comparison to individuals that rear in brackish/saltwater [4, 6]. The hypothesis that phenotypic plasticity alone can account for all of the differences was not supported by three independent controlled experiments [7-10]. Here, we present a genome-wide association study that demonstrates a polygenic basis that discriminates these habitat-specific ecotypes belonging to the same panmictic population. We found that 331 co-varying loci out of 42,424 initially considered were associated with the divergent ecotypes, allowing a reclassification of 89.6%. These 331 SNPs are associated with 101 genes that represent vascular and morphological development, calcium ion regulation, growth and transcription factors, and olfactory receptors. Our results are consistent with divergent natural selection of phenotypes and/or genotype-dependent habitat choice by individuals that results in these genetic differences between habitats, occurring every generation anew in this panmictic species.

Measuring the effects of selection on the genome imposed by human-altered environment is currently a major goal in ecological genomics. Given the polygenic basis of most phenotypic traits, quantitative genetic theory predicts that selection is expected to cause subtle allelic changes among covarying loci rather than pronounced changes at few loci of large effects. The goal of this study was to test for the occurrence of polygenic selection in both North Atlantic eels (European Eel, Anguilla anguilla and American Eel, A. rostrata), using a method that searches for covariation among loci that would discriminate eels from 'control' vs. 'polluted' environments and be associated with specific contaminants acting as putative selective agents. RAD-seq libraries resulted in 23 659 and 14 755 filtered loci for the European and American Eels, respectively. A total of 142 and 141 covarying markers discriminating European and American Eels from 'control' vs. 'polluted' sampling localities were obtained using the Random Forest algorithm. Distance-based redundancy analyses (db-RDAs) were used to assess the relationships between these covarying markers and concentration of 34 contaminants measured for each individual eel. PCB153, 4'4'DDE and selenium were associated with covarying markers for both species, thus pointing to these contaminants as major selective agents in contaminated sites. Gene enrichment analyses suggested that sterol regulation plays an important role in the differential survival of eels in 'polluted' environment. This study illustrates the power of combining methods for detecting signals of polygenic selection and for associating variation of markers with putative selective agents in studies aiming at documenting the dynamics of selection at the genomic level and particularly so in human-altered environments.

The evolution of reproductive isolation in an ecological context may involve multiple facets of species divergence on which divergent selection may operate. These include variation in quantitative phenotypic traits, regulation of gene expression, and differential transmission of particular allelic combinations. Thus, an integrative approach to the speciation process involves identifying the genetic basis of these traits, in order to understand how they are affected by divergent selection in nature and how they ultimately contribute to reproductive isolation. In the Lake Whitefish (Coregonus clupeaformis), dwarf and normal species pairs sympatrically occur in several North American postglacial lakes. The limnetic dwarf whitefish distinguishes from its normal benthic relative by numerous life history, behavioural, morphological and gene expression traits, in relation with the exploitation of distinct ecological niches. Here, we have applied the RAD-Sequencing method to a hybrid backcross family to reconstruct a high-density genetic linkage map and perform QTL mapping in the Lake Whitefish. The 3061 cM map encompassed 3438 segregating RAD markers distributed over 40 linkage groups, for an average resolution of 0.89 cM. We mapped phenotypic and expression QTL underlying ecologically important traits as well as transmission ratio distortion QTL, and identified genomic regions harbouring clusters of such QTL. A narrow genomic region strongly associated with sex determination was also evidenced. Positional and functional information revealed in this study will be useful in ongoing population genomic studies to illuminate our understanding of the genomic architecture of reproductive isolation between whitefish species pairs.

A functional understanding of processes involved in adaptive divergence is one of the awaiting opportunities afforded by high-throughput transcriptomic technologies. Functional analysis of coexpressed genes has succeeded in the biomedical field in identifying key drivers of disease pathways. However, in ecology and evolutionary biology, functional interpretation of transcriptomic data is still limited. Here, we used Weighted Gene Co-Expression Network Analysis (WGCNA) to identify modules of coexpressed genes in muscle and brain tissue of a lake whitefish backcross progeny. Modules were connected to gradients of known adaptive traits involved in the ecological speciation process between benthic and limnetic ecotypes. Key drivers, that is, hub genes of functional modules related to reproduction, growth, and behavior were identified, and module preservation was assessed in natural populations. Using this approach, we identified modules of coexpressed genes involved in phenotypic divergence and their key drivers, and further identified a module part specifically rewired in the backcross progeny. Functional analysis of transcriptomic data can significantly contribute to the understanding of the mechanisms underlying ecological speciation. Our findings point to bone morphogenetic protein and calcium signaling as common pathways involved in coordinated evolution of trophic behavior, trophic morphology (gill rakers), and reproduction. Results also point to pathways implicating hemoglobins and constitutive stress response (HSP70) governing growth in lake whitefish.

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The integration of environmental DNA (eDNA) within management strategies for lotic organisms requires translating eDNA detection and quantification data into inferences of the locations and abundances of target species. Understanding how eDNA is distributed in space and time within the complex environments of rivers and streams is a major factor in achieving this translation. Here we study bidimensional eDNA signals in streams to predict the position and abundance of Atlantic salmon (Salmo salar) juveniles. We use data from sentinel cages with a range of abundances (3–63 juveniles) that were deployed in three coastal streams in New Brunswick, Canada. We evaluate the spatial patterns of eDNA dispersal and determine the effect of discharge on the dilution rate of eDNA. Our results show that eDNA exhibits predictable plume dynamics downstream from sources, with eDNA being initially concentrated and transported in the midstream, but eventually accumulating in stream margins with time and distance. From these findings we developed a fish detection and distribution prediction model based on the eDNA ratio in midstream versus bankside sites for a variety of fish distribution scenarios. Finally, we advise that sampling midstream at every 400 m is sufficient to detect a single fish at low velocity, but sampling efforts need to be increased at higher water velocity (every 100 m in the systems surveyed in this study). Studying salmon eDNA spatio-temporal patterns in lotic environments is essential to developing strong quantitative population assessment models that successfully leverage eDNA as a tool to protect salmon populations.