A lack of genetic diversity and minimal adaptive evolutionary divergence in introduced Mysis shrimp after 50 years.

The successes of introduced populations in novel habitats often provide powerful examples of evolution and adaptation. In the 1950s, opossum shrimp (Mysis diluviana) individuals from Clearwater Lake in Minnesota, USA were transported and introduced to Twin Lakes in Colorado, USA by fisheries managers to supplement food sources for trout. Mysis were subsequently introduced from Twin Lakes into numerous lakes throughout Colorado. Because managers kept detailed records of the timing of the introductions, we had the opportunity to test for evolutionary divergence within a known time interval. Here, we used reduced representation genomic data to investigate patterns of genetic diversity, test for genetic divergence between populations, and for evidence of adaptive evolution within the introduced populations in Colorado. We found very low levels of genetic diversity across all populations, with evidence for some genetic divergence between the Minnesota source population and the introduced populations in Colorado. There was little differentiation among the Colorado populations, consistent with the known provenance of a single founding population, with the exception of the population from Gross Reservoir, Colorado. Demographic modeling suggests that at least one undocumented introduction from an unknown source population hybridized with the population in Gross Reservoir. Despite the overall low genetic diversity we observed, F ST outlier and environmental association analyses identified multiple loci exhibiting signatures of selection and adaptive variation related to elevation and lake depth. The success of introduced species is thought to be limited by genetic variation, but our results imply that populations with limited genetic variation can become established in a wide range of novel environments. From an applied perspective, the observed patterns of divergence between populations suggest that genetic analysis can be a useful forensic tool to determine likely sources of invasive species.

Gut microbiota parallelism and divergence associated with colonisation of novel habitats.

An organism's gut microbiota can change in response to novel environmental conditions, in particular when colonisation of new habitats is accompanied by shifts in the host species' ecology. Here, we investigated the gut microbiota of three lizard species (A. inornata, H. maculata and S. cowlesi) from their ancestral-like habitat in the Chihuahuan desert and two colonised habitats with contrasting geological and ecological compositions: the White Sands and Carrizozo lava flow. The host species and the lizards' environment both shape gut microbiota composition, but host effects were overall stronger. Further, we found evidence that colonisation of the same environment by independent host species led to parallel changes of the gut microbiota, whereas the colonisation of two distinct environments by the same host species led to gut microbiota divergence. Some of the gut microbiota changes that accompanied the colonisation of the White Sands were associated with shifts in diet (based on diet information from previous studies), which is congruent with the general observation that trophic ecology has a strong effect on gut microbiota composition. Our study provides insights into how shifts in host ecology accompanying colonisation of novel environments can affect gut microbiota composition and diversity.

An Integrative Perspective On the Mechanistic Basis of Context- Dependent Species Interactions.

It has long been known that the outcome of species interactions depends on the environmental context in which they occur. Climate change research has sparked a renewed interest in context-dependent species interactions because rapidly changing abiotic environments will cause species interactions to occur in novel contexts and researchers must incorporate this in their predictions of species' responses to climate change. Here, we argue that predicting how the environment will alter the outcome of species interactions requires an integrative biology approach that focuses on the traits, mechanisms, and processes that bridge disciplines such as physiology, biomechanics, ecology, and evolutionary biology. Specifically, we advocate for quantifying how species differ in their tolerance and performance to both environmental challenges independent of species interactions, and in interactions with other species as a function of the environment. Such an approach increases our understanding of the mechanisms underlying outcomes of species interactions across different environmental contexts. This understanding will help determine how the outcome of species interactions affects the relative abundance and distribution of the interacting species in nature. A general theme that emerges from this perspective is that species are unable to maintain high levels of performance across different environmental contexts because of trade-offs between physiological tolerance to environmental challenges and performance in species interactions. Thus, an integrative biology paradigm that focuses on the trade-offs across environments, the physiological mechanisms involved, and how the ecological context impacts the outcome of species interactions provides a stronger framework to understand why species interactions are context dependent.

A genetically based ecological trade-off contributes to setting a geographic range limit.

Understanding the ecological factors that shape geographic range limits and the evolutionary constraints that prevent populations from adaptively evolving beyond these limits is an unresolved question. Here, we investigated why the euryhaline fish, Poecila reticulata, is confined to freshwater within its native range, despite being tolerant of brackish water. We hypothesised that competitive interactions with a close relative, Poecilia picta, in brackish water prevents P. reticulata from colonising brackish water. Using a combination of field transplant, common garden breeding, and laboratory behaviour experiments, we find support for this hypothesis, as P. reticulata are behaviourally subordinate and have lower survival in brackish water with P. picta. We also found a negative genetic correlation between P. reticulata growth in brackish water versus freshwater in the presence of P. picta, suggesting a genetically based trade-off between salinity tolerance and competitive ability could constrain adaptive evolution at the range limit.

Trade-offs, Pleiotropy, and Shared Molecular Pathways: A Unified View of Constraints on Adaptation.

The concept of trade-offs permeates our thinking about adaptive evolution because they are exhibited at every level of biological organization, from molecular and cellular processes to organismal and ecological functions. Trade-offs inevitably arise because different traits do not occur in isolation, but instead are imbedded within complex, integrated systems that make up whole organisms. The genetic and mechanistic underpinning of trade-offs can be found in the pleiotropic nodes that occur in the biological pathways shared between traits. Yet, often trade-offs are only understood as statistical correlations, limiting the ability to evaluate the interplay between how selection and constraint interact during adaptive evolution. Here, we first review the classic paradigms in which physiologists and evolutionary biologists have studied trade-offs and highlight the ways in which network and molecular pathway approaches unify these paradigms. We discuss how these approaches allow researchers to evaluate why trade-offs arise and how selection can act to overcome trait correlations and evolutionary constraints. We argue that understanding how the conserved molecular pathways are shared between different traits and functions provides a conceptual framework for evolutionary biologists, physiologists, and molecular biologists to meaningfully work together toward the goal of understanding why correlations and trade-offs occur between traits. We briefly highlight the melanocortin system and the hormonal control of osmoregulation as two case studies where an understanding of shared molecular pathways reveals why trade-offs occur between seemingly unrelated traits. While we recognize that applying such approaches poses challenges and limitations particularly in the context of natural populations, we advocate for the view that focusing on the biological pathways responsible for trade-offs provides a unified conceptual context accessible to a broad range of integrative biologists.