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.

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.

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.

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.

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.