Blake Matthews

Genomics and the origin of species

Speciation is a fundamental evolutionary process, the knowledge of which is crucial for understanding the origins of biodiversity. Genomic approaches are an increasingly important aspect of this research field. We review current understanding of genome-wide effects of accumulating reproductive isolation and of genomic properties that influence the process of speciation. Building on this work, we identify emergent trends and gaps in our understanding, propose new approaches to more fully integrate genomics into speciation research, translate speciation theory into hypotheses that are testable using genomic tools and provide an integrative definition of the field of speciation genomics.

Evolutionary diversification in stickleback affects ecosystem functioning

Explaining the ecological causes of evolutionary diversification is a major focus of biology, but surprisingly little has been said about the effects of evolutionary diversification on ecosystems. The number of species in an ecosystem and their traits are key predictors of many ecosystem-level processes, such as rates of productivity, biomass sequestration and decomposition. Here we demonstrate short-term ecosystem-level effects of adaptive radiation in the threespine stickleback (Gasterosteus aculeatus) over the past 10,000 years. These fish have undergone recent parallel diversification in several lakes in coastal British Columbia, resulting in the formation of two specialized species (benthic and limnetic) from a generalist ancestor. Using a mesocosm experiment, we demonstrate that this diversification has strong effects on ecosystems, affecting prey community structure, total primary production, and the nature of dissolved organic materials that regulate the spectral properties of light transmission in the system. However, these ecosystem effects do not simply increase in their relative strength with increasing specialization and species richness; instead, they reflect the complex and indirect consequences of ecosystem engineering by sticklebacks. It is well known that ecological factors influence adaptive radiation. We demonstrate that adaptive radiation, even over short timescales, can have profound effects on ecosystems.

Toward an integration of evolutionary biology and ecosystem science

At present, the disciplines of evolutionary biology and ecosystem science are weakly integrated. As a result, we have a poor understanding of how the ecological and evolutionary processes that create, maintain, and change biological diversity affect the flux of energy and materials in global biogeochemical cycles. The goal of this article was to review several research fields at the interfaces between ecosystem science, community ecology and evolutionary biology, and suggest new ways to integrate evolutionary biology and ecosystem science. In particular, we focus on how phenotypic evolution by natural selection can influence ecosystem functions by affecting processes at the environmental, population and community scale of ecosystem organization. We develop an eco-evolutionary model to illustrate linkages between evolutionary change (e.g. phenotypic evolution of producer), ecological interactions (e.g. consumer grazing) and ecosystem processes (e.g. nutrient cycling). We conclude by proposing experiments to test the ecosystem consequences of evolutionary changes.

Genetics of ecological divergence during speciation

Ecological differences often evolve early in speciation as divergent natural selection drives adaptation to distinct ecological niches, leading ultimately to reproductive isolation. Although this process is a major generator of biodiversity, its genetic basis is still poorly understood. Here we investigate the genetic architecture of niche differentiation in a sympatric species pair of threespine stickleback fish by mapping the environment-dependent effects of phenotypic traits on hybrid feeding and performance under semi-natural conditions. We show that multiple, unlinked loci act largely additively to determine position along the major niche axis separating these recently diverged species. We also find that functional mismatch between phenotypic traits reduces the growth of some stickleback hybrids beyond that expected from an intermediate phenotype, suggesting a role for epistasis between the underlying genes. This functional mismatch might lead to hybrid incompatibilities that are analogous to those underlying intrinsic reproductive isolation but depend on the ecological context.

Environmental stability and lake zooplankton diversity – contrasting effects of chemical and thermal variability

Environmental variability in space and time is a primary mechanism allowing species that share resources to coexist. Fluctuating conditions are a double edged sword for diversity, either promoting coexistence through temporal niche partitioning or excluding species by stochastic extinctions. The net effect of environmental variation on diversity is largely unknown. We examined the association between zooplankton species richness in lakes and environmental variability on interannual, seasonal and shorter time scales, as well as long-term average conditions. We analyzed data on physical, chemical and biological limnology in 53 temperate zone lakes in North America and Europe sampled over a combined 1042 years. Large fluctuations in pH, phosphorus and dissolved organic carbon concentration on different time scales were associated with reduced zooplankton species richness. More species were found in lakes that showed greater temperature variation on all time scales. Environmental variability on different time scales showed similar or, in some cases, stronger associations with zooplankton species richness compared with long-term average conditions. Our results suggest that temporal fluctuations in the chemical environment tend to exclude zooplankton species while temperature variability promotes greater richness. The results indicate that anthropogenic increases in temporal variability of future climates may have profound effects on biodiversity.

The ecological forecast horizon, and examples of its uses and determinants

Forecasts of ecological dynamics in changing environments are increasingly important, and are available for a plethora of variables, such as species abundance and distribution, community structure and ecosystem processes. There is, however, a general absence of knowledge about how far into the future, or other dimensions (space, temperature, phylogenetic distance), useful ecological forecasts can be made, and about how features of ecological systems relate to these distances. The ecological forecast horizon is the dimensional distance for which useful forecasts can be made. Five case studies illustrate the influence of various sources of uncertainty (e.g. parameter uncertainty, environmental variation, demographic stochasticity and evolution), level of ecological organisation (e.g. population or community), and organismal properties (e.g. body size or number of trophic links) on temporal, spatial and phylogenetic forecast horizons. Insights from these case studies demonstrate that the ecological forecast horizon is a flexible and powerful tool for researching and communicating ecological predictability. It also has potential for motivating and guiding agenda setting for ecological forecasting research and development.

Under niche construction: an operational bridge between ecology, evolution, and ecosystem science

All living organisms modify their biotic and abiotic environment. Niche construction theory posits that organism-mediated modifications to the environment can change selection pressures and influence the evolutionary trajectories of natural populations. While there is broad support for this proposition in general, there is considerable uncertainty about how niche construction is related to other similar concepts in ecology and evolution. Comparative studies dealing with certain aspects of niche construction are increasingly common, but there is a troubling lack of experimental tests of the core concepts of niche construction theory. Here, we propose an operational framework to evaluate comparative and experimental evidence of the evolutionary consequences of niche construction, and suggest how such research can improve our understanding of ecological and evolutionary dynamics in ecosystems. We advocate for a shift toward explicit experimental tests of how organism-mediated environmental change can influence the selection pressures underlying evolutionary responses, as well as targeted field-based comparative research to identify the mode of evolution by niche construction and assess its importance in natural populations.

Specialization of trophic position and habitat use by sticklebacks in an adaptive radiation

Divergence in habitat use among closely related species is a common characteristic of adaptive radiations. Large differences in the size structure of prey between habitats could strengthen disruptive selection on generalist predators and lead to a divergence in trophic position among species in an adaptive radiation. Using threespine stickleback (Gasterosteus aculeatus) in freshwater lakes as a model system, we examined whether divergence in habitat use coincides with shifts in trophic position. We examined the habitat use and trophic position of individual sticklebacks from divergent lake environments that have only one stickleback species (allopatric lakes) and from lakes that have a pair of benthic and limnetic stickleback species (sympatric lakes). In two sympatric lakes, the limnetic species had a higher trophic position than the benthic species, and in both allopatric and sympatric lakes, sticklebacks specializing on pelagic prey had a higher trophic position for a given size than sticklebacks specializing on benthic prey. Furthermore, the trophic position of pelagic specialists was correlated with individual variation in their gill raker length. Our results indicate that gill raker length is an important trait that underlies differentiation in both habitat use and trophic position among stickleback species, populations, and individuals.

Does human activity impact the natural antibiotic resistance background? Abundance of antibiotic resistance genes in 21 Swiss lakes.

Antibiotic resistance genes (ARGs) are emerging environmental contaminants, known to be continuously discharged into the aquatic environment via human and animal waste. Freshwater aquatic environments represent potential reservoirs for ARG and potentially allow sewage-derived ARG to persist and spread in the environment. This may create increased opportunities for an eventual contact with, and gene transfer to, human and animal pathogens via the food chain or drinking water. However, assessment of this risk requires a better understanding of the level and variability of the natural resistance background and the extent of the human impact. We have analyzed water samples from 21 Swiss lakes, taken at sampling points that were not under the direct influence of local contamination sources and analyzed the relative abundance of ARG using quantitative real-time PCR. Copy numbers of genes mediating resistance to three different broad-spectrum antibiotic classes (sulfonamides: sul1, sul2, tetracyclines: tet(B), tet(M), tet(W) and fluoroquinolones: qnrA) were normalized to copy numbers of bacterial 16S rRNA genes. We used multiple linear regression to assess if ARG abundance is related to human activities in the catchment, microbial community composition and the eutrophication status of the lakes. Sul genes were detected in all sampled lakes, whereas only four lakes contained quantifiable numbers of tet genes, and qnrA remained below detection in all lakes. Our data indicate higher abundance of sul1 in lakes with increasing number and capacity of wastewater treatment plants (WWTPs) in the catchment. sul2 abundance was rather related to long water residence times and eutrophication status. Our study demonstrates the potential of freshwater lakes to preserve antibiotic resistance genes, and provides a reference for ARG abundance from lake systems with low human impact as a baseline for assessing ARG contamination in lake water.

Effects of environmental variation and spatial distance on Bacteria, Archaea and viruses in sub-polar and arctic waters

We investigated the influence of environmental parameters and spatial distance on bacterial, archaeal and viral community composition from 13 sites along a 3200-km long voyage from Halifax to Kugluktuk (Canada) through the Labrador Sea, Baffin Bay and the Arctic Archipelago. Variation partitioning was used to disentangle the effects of environmental parameters, spatial distance and spatially correlated environmental parameters on prokaryotic and viral communities. Viral and prokaryotic community composition were related in the Labrador Sea, but were independent of each other in Baffin Bay and the Arctic Archipelago. In oceans, the dominant dispersal mechanism for prokaryotes and viruses is the movement of water masses, thus, dispersal for both groups is passive and similar. Nevertheless, spatial distance explained 7–19% of the variation in viral community composition in the Arctic Archipelago, but was not a significant predictor of bacterial or archaeal community composition in either sampling area, suggesting a decoupling of the processes regulating community composition within these taxonomic groups. According to the metacommunity theory, patterns in bacterial and archaeal community composition suggest a role for species sorting, while patterns of virus community composition are consistent with species sorting in the Labrador Sea and suggest a potential role of mass effects in the Arctic Archipelago. Given that, a specific prokaryotic taxon may be infected by multiple viruses with high reproductive potential, our results suggest that viral community composition was subject to a high turnover relative to prokaryotic community composition in the Arctic Archipelago.