Pathogen-induced rapid evolution in a vertebrate life-history trait.

Anthropogenic factors, including climate warming, are increasing the incidence and prevalence of infectious diseases worldwide. Infectious diseases caused by pathogenic parasites can have severe impacts on host survival, thereby altering the selection regime and inducing evolutionary responses in their hosts. Knowledge about such evolutionary consequences in natural populations is critical to mitigate potential ecological and economic effects. However, studies on pathogen-induced trait changes are scarce and the pace of evolutionary change is largely unknown, particularly in vertebrates. Here, we use a time series from long-term monitoring of perch to estimate temporal trends in the maturation schedule before and after a severe pathogen outbreak. We show that the disease induced a phenotypic change from a previously increasing to a decreasing size at maturation, the most important life-history transition in animals. Evolutionary rates imposed by the pathogen were high and comparable to those reported for populations exposed to intense human harvesting. Pathogens thus represent highly potent drivers of adaptive phenotypic evolution in vertebrates.

Antagonistic selection from predators and pathogens alters food-web structure.

Selection can alter predator-prey interactions. However, whether and how complex food-webs respond to selection remain largely unknown. We show in the field that antagonistic selection from predators and pathogens on prey body-size can be a primary driver of food-web functioning. In Windermere, U.K., pike (Esox lucius, the predator) selected against small perch (Perca fluviatilis, the prey), while a perch-specific pathogen selected against large perch. The strongest selective force drove perch trait change and ultimately determined the structure of trophic interactions. Before 1976, the strength of pike-induced selection overrode the strength of pathogen-induced selection and drove a change to larger, faster growing perch. Predation-driven increase in the proportion of large, infection-vulnerable perch presumably favored the pathogen since a peak in the predation pressure in 1976 coincided with pathogen expansion and a massive perch kill. After 1976, the strength of pathogen-induced selection overrode the strength of predator-induced selection and drove a rapid change to smaller, slower growing perch. These changes made perch easier prey for pike and weaker competitors against juvenile pike, ultimately increasing juvenile pike survival and total pike numbers. Therefore, although predators and pathogens exploited the same prey in Windermere, they did not operate competitively but synergistically by driving rapid prey trait change in opposite directions. Our study empirically demonstrates that a consideration of the relative strengths and directions of multiple selective pressures is needed to fully understand community functioning in nature.

Harvest-induced disruptive selection increases variance in fitness-related traits.

The form of Darwinian selection has important ecological and management implications. Negative effects of harvesting are often ascribed to size truncation (i.e. strictly directional selection against large individuals) and resultant decrease in trait variability, which depresses capacity to buffer environmental change, hinders evolutionary rebound and ultimately impairs population recovery. However, the exact form of harvest-induced selection is generally unknown and the effects of harvest on trait variability remain unexplored. Here we use unique data from the Windermere (UK) long-term ecological experiment to show in a top predator (pike, Esox lucius) that the fishery does not induce size truncation but disruptive (diversifying) selection, and does not decrease but rather increases variability in pike somatic growth rate and size at age. This result is supported by complementary modelling approaches removing the effects of catch selectivity, selection prior to the catch and environmental variation. Therefore, fishing most likely increased genetic variability for somatic growth in pike and presumably favoured an observed rapid evolutionary rebound after fishery relaxation. Inference about the mechanisms through which harvesting negatively affects population numbers and recovery should systematically be based on a measure of the exact form of selection. From a management perspective, disruptive harvesting necessitates combining a preservation of large individuals with moderate exploitation rates, and thus provides a comprehensive tool for sustainable exploitation of natural resources.

The ideal free pike: 50 years of fitness-maximizing dispersal in Windermere.

The ideal free distribution (IFD) theory is one of the most influential theories in evolutionary ecology. It predicts how animals ought to distribute themselves within a heterogeneous habitat in order to maximize lifetime fitness. We test the population level consequence of the IFD theory using 40-year worth data on pike (Esox lucius) living in a natural lake divided into two basins. We do so by employing empirically derived density-dependent survival, dispersal and fecundity functions in the estimation of basin-specific density-dependent fitness surfaces. The intersection of the fitness surfaces for the two basins is used for deriving expected spatial distributions of pike. Comparing the derived expected spatial distributions with 50 years data of the actual spatial distribution demonstrated that pike is ideal free distributed within the lake. In general, there was a net migration from the less productive north basin to the more productive south basin. However, a pike density-manipulation experiment imposing shifting pike density gradients between the two basins managed to switch the net migration direction and hence clearly demonstrated that the Windermere pike choose their habitat in an ideal free manner. Demonstration of ideal free habitat selection on an operational field scale like this has never been undertaken before.

Trait changes in a harvested population are driven by a dynamic tug-of-war between natural and harvest selection.

Selective harvest of large individuals should alter natural adaptive landscapes and drive evolution toward reduced somatic growth and increased reproductive investment. However, few studies have simultaneously considered the relative importance of artificial and natural selection in driving trait changes in wild populations. Using 50 years of individual-based data on Windermere pike (Esox lucius), we show that trait changes tracked the adaptive peak, which moved in the direction imposed by the dominating selective force. Individual lifetime somatic growth decreased at the start of the time series because harvest selection was strong and natural selection was too weak to override the strength of harvest selection. However, natural selection favoring fast somatic growth strengthened across the time series in parallel with the increase in pike abundance and, presumably, cannibalism. Harvest selection was overridden by natural selection when the fishing effort dwindled, triggering a rapid increase in pike somatic growth. The two selective forces appear to have acted in concert during only one short period of prey collapse that favored slow-growing pike. Moreover, increased somatic growth occurred concurrently with a reduction in reproductive investment in young and small female pike, indicating a tradeoff between growth and reproduction. The age-specific amplitude of this change paralleled the age-specific strength of harvest pressure, suggesting that reduced investment was also a response to increased life expectancy. This is the first study to demonstrate that a consideration of both natural selection and artificial selection is needed to fully explain time-varying trait dynamics in harvested populations.