Ecological speciation in European whitefish is driven by a large-gaped predator.

Lake-dwelling fish that form species pairs/flocks characterized by body size divergence are important model systems for speciation research. Although several sources of divergent selection have been identified in these systems, their importance for driving the speciation process remains elusive. A major problem is that in retrospect, we cannot distinguish selection pressures that initiated divergence from those acting later in the process. To address this issue, we studied the initial stages of speciation in European whitefish (Coregonus lavaretus) using data from 358 populations of varying age (26-10,000 years). We find that whitefish speciation is driven by a large-growing predator, the northern pike (Esox lucius). Pike initiates divergence by causing a largely plastic differentiation into benthic giants and pelagic dwarfs: ecotypes that will subsequently develop partial reproductive isolation and heritable differences in gill raker number. Using an eco-evolutionary model, we demonstrate how pike's habitat specificity and large gape size are critical for imposing a between-habitat trade-off, causing prey to mature in a safer place or at a safer size. Thereby, we propose a novel mechanism for how predators may cause dwarf/giant speciation in lake-dwelling fish species.

Holocene extinctions of a top predator-Effects of time, habitat area and habitat subdivision.

Loss of habitat and changes in the spatial configuration of habitats are major drivers of species extinctions, but the responses to these drivers differ between organisms. To advance theory on how extinction risk from different types of habitat alteration relates to species-specific traits, there is a need for studies of the long-term extinction dynamic of individual species. The goal of this study was to quantify how habitat area and the spatial configuration of habitats affect extinction rate of an aquatic top predator, the northern pike Esox lucius L. We recorded the presence/absence of northern pike in 398 isolated habitat fragments, each one consisting of a number of interconnected lakes. Time since isolation of the habitat fragments, caused by cut-off from the main dispersal source in the Baltic Sea, varied between 0 and 10,000 years. Using survival regression, we analysed how pike population survival was affected by time since isolation, habitat size and habitat subdivision. The approach builds on the assumptions that pike colonized all fragments before isolation and that current absences result from extinctions. We verified these assumptions by testing (a) if pike was present in the region throughout the entire time period when the lakes formed and (b) if pike typically colonize lakes that are formed today. We also addressed the likelihood that unrecorded anthropogenic introductions could bias our estimates of extinction rate. Our results supported the interpretation that current patterns of presence/absence in our study system are shaped by extinctions. Further, we found that time since isolation and fragment area had strong effects on pike population survival. In contrast, spatial habitat subdivision (i.e. if a fragment contained few large lakes or many small lakes) and other environmental covariates describing climate and productivity were unrelated to pike survival. Over all, extinction rate was high in young fragments and decreased sharply with increasing fragment age. Our study demonstrates how the link between extinction rate and habitat size and spatial structure can be quantified. More similar studies may help us find generalizations that can guide management of habitat size and connectivity.

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.

Biotic and abiotic drivers of species loss rate in isolated lakes.

Today, anthropogenic impacts are causing a serious crisis for global biodiversity, with rates of extinction increasing at an unprecedented rate. Extinctions typically occur after a certain delay, and understanding the mechanisms causing delays is a key challenge for both fundamental and applied perspectives. Here, we make use of natural experiments, the isolation of lakes by land uplift in Northern Scandinavia, to examine how yearly extinction rates are affected by time since isolation and a range of abiotic and biotic factors. In this aim, we adapted a model of delayed species loss within isolated communities to test the effects of time since isolation, area, pH, depth and the presence/absence of piscivores on extinction rates. As expected, we found that small and/or young lakes experience a higher annual rate of extinctions per species than larger and/or older ones. Compared to previous studies that were conducted for either young (few thousand years ago) or very old (>10,000 years ago) isolates, we demonstrated over a large and continuous temporal scales (50-5,000 years), similar relationship between extinction rates and age. We also show that extinction rates are modified by local environmental factors such as a strong negative effect of increasing pH. Our results urge for the need to consider the time since critical environmental changes occurred when studying extinction rates. In a wider perspective, our study demonstrates the need to consider extinction debts when modelling future effects of climate change, land-use changes or biological invasions on biodiversity.

Environmental DNA Time Series in Ecology.

Ecological communities change in time and space, but long-term dynamics at the century-to-millennia scale are poorly documented due to lack of relevant data sets. Nevertheless, understanding long-term dynamics is important for explaining present-day biodiversity patterns and placing conservation goals in a historical context. Here, we use recent examples and new perspectives to highlight how environmental DNA (eDNA) is starting to provide a powerful new source of temporal data for research questions that have so far been overlooked, by helping to resolve the ecological dynamics of populations, communities, and ecosystems over hundreds to thousands of years. We give examples of hypotheses that may be addressed by temporal eDNA biodiversity data, discuss possible research directions, and outline related challenges.

Effects of warming on predator-prey interactions - a resource-based approach and a theoretical synthesis.

We theoretically explore consequences of warming for predator-prey dynamics, broadening previous approaches in three ways: we include beyond-optimal temperatures, predators may have a type III functional response, and prey carrying capacity depends on explicitly modelled resources. Several robust patterns arise. The relationship between prey carrying capacity and temperature can range from near-independence to monotonically declining/increasing to hump-shaped. Predators persist in a U-shaped region in resource supply (=enrichment)-temperature space. Type II responses yield stable persistence in a U-shaped band inside this region, giving way to limit cycles with enrichment at all temperatures. In contrast, type III responses convey stability at intermediate temperatures and confine cycles to low and high temperatures. Warming-induced state shifts can be predicted from system trajectories crossing stability and persistence boundaries in enrichment-temperature space. Results of earlier studies with more restricted assumptions map onto this graph as special cases. Our approach thus provides a unifying framework for understanding warming effects on trophic dynamics.

Strong invaders are strong defenders - implications for the resistance of invaded communities.

Many ecosystems receive a steady stream of non-native species. How biotic resistance develops over time in these ecosystems will depend on how established invaders contribute to subsequent resistance. If invasion success and defence capacity (i.e. contribution to resistance) are correlated, then community resistance should increase as species accumulate. If successful invaders also cause most impact (through replacing native species with low defence capacity) then the effect will be even stronger. If successful invaders instead have weak defence capacity or even facilitative attributes, then resistance should decrease with time, as proposed by the invasional meltdown hypothesis. We analysed 1157 introductions of freshwater fish in Swedish lakes and found that species' invasion success was positively correlated with their defence capacity and impact, suggesting that these communities will develop stronger resistance over time. These insights can be used to identify scenarios where invading species are expected to cause large impact.

Weighted species richness outperforms species richness as predictor of biotic resistance.

The species richness hypothesis, which predicts that species-rich communities should be better at resisting invasions than species-poor communities, has been empirically tested many times and is often poorly supported. In this study, we contrast the species richness hypothesis with four alternative hypotheses with the aim of finding better descriptors of invasion resistance. These alternative hypotheses state that resistance to invasions is determined by abiotic conditions, community saturation (i.e., the number of resident species relative to the maximum number of species that can be supported), presence/absence of key species, or weighted species richness. Weighted species richness is a weighted sum of the number of species, where each species' weight describes its contribution to resistance. We tested these hypotheses using data on the success of 571 introductions of four freshwater fish species into lakes throughout Sweden, i.e., Arctic char (Salvelinus alpinus), tench (Tinca tinca), zander (Sander lucioperca), and whitefish (Coregonus lavaretus). We found that weighted species richness best predicted invasion success. The weights describing the contribution of each resident species to community resistance varied considerably in both strength and sign. Positive resistance weights, which indicate that species repel invaders, were as common as negative resistance weights, which indicate facilitative interactions. This result can be contrasted with the implicit assumption of the original species richness hypothesis, that all resident species have negative effects on invader success. We argue that this assumption is unlikely to be true in natural communities, and thus that we expect that weighted species richness is a better predictor of invader success than the actual number of resident species.

Mechanisms by Which Phenotypic Plasticity Affects Adaptive Divergence and Ecological Speciation.

Phenotypic plasticity is the ability of one genotype to produce different phenotypes depending on environmental conditions. Several conceptual models emphasize the role of plasticity in promoting reproductive isolation and, ultimately, speciation in populations that forage on two or more resources. These models predict that plasticity plays a critical role in the early stages of speciation, prior to genetic divergence, by facilitating fast phenotypic divergence. The ability to plastically express alternative phenotypes may, however, interfere with the early phase of the formation of reproductive barriers, especially in the absence of geographic barriers. Here, we quantitatively investigate mechanisms under which plasticity can influence progress toward adaptive genetic diversification and ecological speciation. We use a stochastic, individual-based model of a predator-prey system incorporating sexual reproduction and mate choice in the predator. Our results show that evolving plasticity promotes the evolution of reproductive isolation under diversifying environments when individuals are able to correctly select a more profitable habitat with respect to their phenotypes (i.e., adaptive habitat choice) and to assortatively mate with relatively similar phenotypes. On the other hand, plasticity facilitates the evolution of plastic generalists when individuals have a limited capacity for adaptive habitat choice. We conclude that plasticity can accelerate the evolution of a reproductive barrier toward adaptive diversification and ecological speciation through enhanced phenotypic differentiation between diverging phenotypes.

Space race functional responses.

We derive functional responses under the assumption that predators and prey are engaged in a space race in which prey avoid patches with many predators and predators avoid patches with few or no prey. The resulting functional response models have a simple structure and include functions describing how the emigration of prey and predators depend on interspecific densities. As such, they provide a link between dispersal behaviours and community dynamics. The derived functional response is general but is here modelled in accordance with empirically documented emigration responses. We find that the prey emigration response to predators has stabilizing effects similar to that of the DeAngelis-Beddington functional response, and that the predator emigration response to prey has destabilizing effects similar to that of the Holling type II response. A stability criterion describing the net effect of the two emigration responses on a Lotka-Volterra predator-prey system is presented. The winner of the space race (i.e. whether predators or prey are favoured) is determined by the relationship between the slopes of the species' emigration responses. It is predicted that predators win the space race in poor habitats, where predator and prey densities are low, and that prey are more successful in richer habitats.

Temperature dependence of predation depends on the relative performance of predators and prey.

The temperature dependence of predation rates is a key issue for understanding and predicting the responses of ecosystems to climate change. Using a simple mechanistic model, we demonstrate that differences in the relative performances of predator and prey can cause strong threshold effects in the temperature dependence of attack rates. Empirical data on the attack rate of northern pike (Esox lucius) feeding on brown trout (Salmo trutta) confirm this result. Attack rates fell sharply below a threshold temperature of +11°C, which corresponded to a shift in relative performance of pike and brown trout with respect to maximum attack and escape swimming speeds. The average attack speed of pike was an order of magnitude lower than the escape speed of brown trout at 5°C, but approximately equal at temperatures above 11°C. Thresholds in the temperature dependence of ecological rates can create tipping points in the responses of ecosystems to increasing temperatures. Thus, identifying thresholds is crucial when predicting future effects of climate warming.

Assessing anthropogenic impact on boreal lakes with historical fish species distribution data and hydrogeochemical modeling.

Quantifying the effects of human activity on the natural environment is dependent on credible estimates of reference conditions to define the state of the environment before the onset of adverse human impacts. In Europe, emission controls that aimed at restoring ecological status were based on hindcasts from process-based models or paleolimnological reconstructions. For instance, 1860 is used in Europe as the target for restoration from acidification concerning biological and chemical parameters. A more practical problem is that the historical states of ecosystems and their function cannot be observed directly. Therefore, we (i) compare estimates of acidification based on long-term observations of roach (Rutilus rutilus) populations with hindcast pH from the hydrogeochemical model MAGIC; (ii) discuss policy implications and possible scope for use of long-term archival data for assessing human impacts on the natural environment and (iii) present a novel conceptual model for interpreting the importance of physico-chemical and ecological deviations from reference conditions. Of the 85 lakes studied, 78 were coherently classified by both methods. In 1980, 28 lakes were classified as acidified with the MAGIC model, however, roach was present in 14 of these. In 2010, MAGIC predicted chemical recovery in 50% of the lakes, however roach only recolonized in five lakes after 1990, showing a lag between chemical and biological recovery. Our study is the first study of its kind to use long-term archival biological data in concert with hydrogeochemical modeling for regional assessments of anthropogenic acidification. Based on our results, we show how the conceptual model can be used to understand and prioritize management of physico-chemical and ecological effects of anthropogenic stressors on surface water quality.

Fish introductions reveal the temperature dependence of species interactions.

A major area of current research is to understand how climate change will impact species interactions and ultimately biodiversity. A variety of environmental conditions are rapidly changing owing to climate warming, and these conditions often affect both the strength and outcome of species interactions. We used fish distributions and replicated fish introductions to investigate environmental conditions influencing the coexistence of two fishes in Swedish lakes: brown trout (Salmo trutta) and pike (Esox lucius). A logistic regression model of brown trout and pike coexistence showed that these species coexist in large lakes (more than 4.5 km(2)), but not in small, warm lakes (annual air temperature more than 0.9-1.5°C). We then explored how climate change will alter coexistence by substituting climate scenarios for 2091-2100 into our model. The model predicts that brown trout will be extirpated from approximately half of the lakes where they presently coexist with pike and from nearly all 9100 lakes where pike are predicted to invade. Context dependency was critical for understanding pike-brown trout interactions, and, given the widespread occurrence of context-dependent species interactions, this aspect will probably be critical for accurately predicting climate impacts on biodiversity.

Population-level consequences of heterospecific density-dependent movements in predator-prey systems.

In this paper we elucidate how small-scale movements, such as those associated with searching for food and avoiding predators, affect the stability of predator-prey dynamics. We investigate an individual-based Lotka-Volterra model with density-dependent movement, in which the predator and prey populations live in a very large number of coupled patches. The rates at which individuals leave patches depend on the local densities of heterospecifics, giving rise to one reaction norm for each of the two species. Movement rates are assumed to be much faster than demographics rates. A spatial structure of predators and prey emerges which affects the global population dynamics. We derive a criterion which reveals how demographic stability depends on the relationships between the per capita covariance and densities of predators and prey. Specifically, we establish that a positive relationship with prey density and a negative relationship with predator density tend to be stabilizing. On a more mechanistic level we show how these relationships are linked to the movement reaction norms of predators and prey. Numerical results show that these findings hold both for local and global movements, i.e., both when migration is biased towards neighbouring patches and when all patches are reached with equal probability.

Future distribution of Arctic char Salvelinus alpinus in Sweden under climate change: effects of temperature, lake size and species interactions.

Novel communities will be formed as species with a variety of dispersal abilities and environmental tolerances respond individually to climate change. Thus, models projecting future species distributions must account for species interactions and differential dispersal abilities. We developed a species distribution model for Arctic char Salvelinus alpinus, a freshwater fish that is sensitive both to warm temperatures and to species interactions. A logistic regression model using lake area, mean annual air temperature (1961-1990), pike Esox lucius and brown trout Salmo trutta occurrence correctly classified 95 % of 467 Swedish lakes. We predicted that Arctic char will lose 73 % of its range in Sweden by 2100. Predicted extinctions could be attributed both to simulated temperature increases and to projected pike invasions. The Swedish mountains will continue to provide refugia for Arctic char in the future and should be the focus of conservation efforts for this highly valued fish.

Functional responses and scaling in predator-prey interactions of marine fishes: contemporary issues and emerging concepts.

Predator-prey interactions are a primary structuring force vital to the resilience of marine communities and sustainability of the world's oceans. Human influences on marine ecosystems mediate changes in species interactions. This generality is evinced by the cascading effects of overharvesting top predators on the structure and function of marine ecosystems. It follows that ecological forecasting, ecosystem management, and marine spatial planning require a better understanding of food web relationships. Characterising and scaling predator-prey interactions for use in tactical and strategic tools (i.e. multi-species management and ecosystem models) are paramount in this effort. Here, we explore what issues are involved and must be considered to advance the use of predator-prey theory in the context of marine fisheries science. We address pertinent contemporary ecological issues including (1) the approaches and complexities of evaluating predator responses in marine systems; (2) the 'scaling up' of predator-prey interactions to the population, community, and ecosystem level; (3) the role of predator-prey theory in contemporary fisheries and ecosystem modelling approaches; and (4) directions for the future. Our intent is to point out needed research directions that will improve our understanding of predator-prey interactions in the context of the sustainable marine fisheries and ecosystem management.

Morphological and genetic divergence in Swedish postglacial stickleback (Pungitius pungitius) populations.

BACKGROUND: An important objective of evolutionary biology is to understand the processes that govern phenotypic variation in natural populations. We assessed patterns of morphological and genetic divergence among coastal and inland lake populations of nine-spined stickleback in northern Sweden. Coastal populations are either from the Baltic coast (n = 5) or from nearby coastal lakes (n = 3) that became isolated from the Baltic Sea (< 100 years before present, ybp). Inland populations are from freshwater lakes that became isolated from the Baltic approximately 10,000 ybp; either single species lakes without predators (n = 5), or lakes with a recent history of predation (n = 5) from stocking of salmonid predators (~50 ybp). RESULTS: Coastal populations showed little variation in 11 morphological traits and had longer spines per unit of body length than inland populations. Inland populations were larger, on average, and showed greater morphological variation than coastal populations. A principal component analysis (PCA) across all populations revealed two major morphological axes related to spine length (PC1, 47.7% variation) and body size (PC2, 32.9% variation). Analysis of PCA scores showed marked similarity in coastal (Baltic coast and coastal lake) populations. PCA scores indicate that inland populations with predators have higher within-group variance in spine length and lower within-group variance in body size than inland populations without predators. Estimates of within-group PST (a proxy for QST) from PCA scores are similar to estimates of FST for coastal lake populations but PST >FST for Baltic coast populations. PST >FST for PC1 and PC2 for inland predator and inland no predator populations, with the exception that PST

Temperature dependence of the functional response.

The Arrhenius equation has emerged as the favoured model for describing the temperature dependence of consumption in predator-prey models. To examine the relevance of this equation, we undertook a meta-analysis of published relationships between functional response parameters and temperature. We show that, when plotted in lin-log space, temperature dependence of both attack rate and maximal ingestion rate exhibits a hump-shaped relationship and not a linear one as predicted by the Arrhenius equation. The relationship remains significantly downward concave even when data from temperatures above the peak of the hump are discarded. Temperature dependence is stronger for attack rate than for maximal ingestion rate, but the thermal optima are not different. We conclude that the use of the Arrhenius equation to describe consumption in predator-prey models requires the assumption that temperatures above thermal optima are unimportant for population and community dynamics, an assumption that is untenable given the available data.

Predation leads to assembly rules in fragmented fish communities.

Diamond [Assembly of species communities. In: Ecology and Evolution of Communities (eds Cody, M.L. & Diamond, J.M.). Harvard University Press, Cambridge, pp. 342-444] proposed that resource competition leads to checkerboard-like distributions of competing species. This proposal prompted research that revealed checkerboard patterns within a wide range of communities, but the mechanisms that generate such patterns are still poorly understood. Here we present whole-lake natural experiments and analyses of species-environment relationships in small coastal lake fish communities that were fragmented when land uplift isolated these lakes from the Baltic Sea, showing that a combination of predation and habitat suitability generated checkerboard distributions. Checkerboard patterns developed because two piscivores, northern pike and Eurasian perch, caused the extinction of several prey species in deep lakes. Conversely, low oxygen levels in shallow lakes caused extinction of the piscivores, and these areas served as a refuge for tolerant prey species. Based on these findings, we suggest that habitat suitability and biotic interactions should be viewed simultaneously in null models of assembly rules.

Contrasting effects of anthropogenic and natural acidity in streams: a meta-analysis.

Large-scale human activities including the extensive combustion of fossil fuels have caused acidification of freshwater systems on a continental scale, resulting in reduced species diversity and, in some instances, impaired ecological functioning. In regions where acidity is natural, however, species diversity and functioning seem to be less affected. This contrasting response is likely to have more than one explanation including the possibility of adaptation in organisms exposed to natural acidity over evolutionary time scales and differential toxicity due to dissimilarities in water chemistry other than pH. However, empirical evidence supporting these hypotheses is equivocal. Partly, this is because previous research has mainly been conducted at relatively small geographical scales, and information on ecological functioning in this context is generally scarce. Our goal was to test whether anthropogenic acidity has stronger negative effects on species diversity and ecological functioning than natural acidity. Using a meta-analytic approach based on 60 datasets, we show that macroinvertebrate species richness and the decomposition of leaf litter -- an important process in small streams -- tend to decrease with increasing acidity across regions and across both the acidity categories. Macroinvertebrate species richness, however, declines three times more rapidly with increasing acidity where it is anthropogenic than where it is natural, in agreement with the adaptation hypothesis and the hypothesis of differences in water chemistry. By contrast, the loss in ecological functioning differs little between the categories, probably because increases in the biomass of taxa remaining at low pH compensate for losses in functionality that would otherwise accompany losses of taxa from acidic systems. This example from freshwater acidification illustrates how natural and anthropogenic stressors can differ markedly in their effects on species diversity and one aspect of ecological functioning.