Signals of predation-induced directional and disruptive selection in the threespine stickleback (original) (raw)
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Intraguild predation leads to genetically based character shifts in the threespine stickleback
Evolution; international journal of organic evolution, 2015
Intraguild predation is a common ecological interaction that occurs when a species preys upon another species with which it competes. The interaction is potentially a mechanism of divergence between intraguild prey populations, but it is unknown if cases of character shifts in intraguild prey are an environmental or evolutionary response. We investigated the genetic basis and inducibility of character shifts in threespine stickleback from lakes with and without prickly sculpin, a benthic intraguild predator. Wild populations of stickleback sympatric with sculpin repeatedly show greater defensive armor and water column height preference. We lab-raised stickleback from lakes with and without sculpin, as well as marine stickleback, and found that differences between populations in armor, body shape, and behavior persisted in a common garden. Within the common garden, we raised stickleback half-families from multiple populations in the presence and absence of sculpin. Although the prese...
Ecological causes of morphological evolution in the three-spined stickleback
Ecology and evolution, 2013
The central assumption of evolutionary theory is that natural selection drives the adaptation of populations to local environmental conditions, resulting in the evolution of adaptive phenotypes. The three-spined stickleback (Gasterosteus aculeatus) displays remarkable phenotypic variation, offering an unusually tractable model for understanding the ecological mechanisms underpinning adaptive evolutionary change. Using populations on North Uist, Scotland we investigated the role of predation pressure and calcium limitation on the adaptive evolution of stickleback morphology and behavior. Dissolved calcium was a significant predictor of plate and spine morph, while predator abundance was not. Stickleback latency to emerge from a refuge varied with morph, with populations with highly reduced plates and spines and high predation risk less bold. Our findings support strong directional selection in three-spined stickleback evolution, driven by multiple selective agents.
TEMPORAL VARIATION IN DIVERGENT SELECTION ON SPINE NUMBER IN THREESPINE STICKLEBACK
Evolution, 2002
Short-term temporal cycles in ecological pressures, such as shifts in predation regime, are widespread in nature yet estimates of temporal variation in the direction and intensity of natural selection are few. Previous work on threespine stickleback (Gasterosteus aculeatus) has revealed that dorsal and pelvic spines are a defense against gape-limited predators but may be detrimental against grappling insect predators. In this study, we examined a 15year database from an endemic population of threespine stickleback to look for evidence of temporal shifts in exposure to these divergent predation regimes and correlated shifts in selection on spine number. For juveniles, we detected selection for increased spine number during winter when gape-limited avian piscivores were most common but selection for decreased spine number during summer when odonate predation was more common. For subadults and adults, which are taken primarily by avian piscivores, we predicted selection should generally be for increased spine number in all seasons. Among 59 comparisons, four selection differentials were significant (Bonferroni corrected) and in the predicted direction. However, there was also substantial variability in remaining differentials, including two examples with strong selection for spine reduction. These reversals were associated with increased tendency of the fish to shift to a benthic niche, as determined from examination of stomach contents. These dietary data suggest that increased encounter rates with odonate predation select for spine reduction. Strong selection on spine number was followed by changes in mean spine number during subsequent years and a standard quantitative genetic formula revealed that spine number has a heritable component. Our results provide evidence of rapid morphological responses to selection from predators and suggest that temporal variation in selection may help maintain variation within populations. Furthermore, our findings indicate that variable selection can be predicted if the agents of selection are known.
Heredity, 1973
Sticklebacks in Lakes Wapato and Chelan are far inland and highly isolated from other populations. They live about one year. Rainbow trout prey on sticklebacks most heavily during the winter, and this predation is random on males and females and on the three plate morphs. However, trout show strong selective predation on sticklebacks with respect to plate number. The selective advantage of seven plated sticklebacks under predation is highly significant and consistent over three years. The frequency of seven plated adults in Lake Wapato was 56 per cent, in 1968, but increased to 65 per cent, in 1969 and has since remained at about 62 per cent. This large increase coincides with the time interval when predation was heaviest and when selective predation favouring sevens was greatest. The heritabilities for number of plates and gill rakers are high, and so the values obtained for the increase in mean relative fitness show that natural selection is acting strongly on these traits. Predation acting on the variation in plate number and food specialisation acting on gill rakers are two of the major selective agents.
Intraguild Predation Drives Evolutionary Niche Shift in Threespine Stickleback
Evolution, 2012
Intraguild predation-competition and predation by the same antagonist-is widespread, but its evolutionary consequences are unknown. Intraguild prey may evolve antipredator defenses, superior competitive ability on shared resources, or the ability to use an alternative resource, any of which may alter the structure of the food web. We tested for evolutionary responses by threespine stickleback to a benthic intraguild predator, prickly sculpin. We used a comparative morphometric analysis to show that stickleback sympatric with sculpin are more armored and have more limnetic-like body shapes than allopatric stickleback. To test the ecological implications of this shift, we conducted a mesocosm experiment that varied sculpin presence and stickleback population of origin (from one sympatric and one allopatric lake). Predation by sculpin greatly increased the mortality of allopatric stickleback. In contrast, sculpin presence did not affect the mortality of sympatric stickleback, although they did have lower growth rates suggesting increased nonpredatory effects of sculpin. Consistent with their morphology, sympatric stickleback included more pelagic prey in their diets, leading to depletion of zooplankton in the mesocosms. These findings suggest that intraguild prey evolution has altered food web structure by reducing both predation by the intraguild predator and diet overlap between species.
Strong and consistent natural selection associated with armour reduction in sticklebacks
Molecular Ecology, 2011
Measuring the strength of natural selection is tremendously important in evolutionary biology, but remains a challenging task. In this work, we analyse the characteristics of selection for a morphological change (lateral-plate reduction) in the threespine stickleback Gasterosteus aculeatus. Adaptation to freshwater, leading with the reduction or loss of the bony lateral armour, has occurred in parallel on numerous occasions in this species. Completely-plated and low-plated sticklebacks were introduced into a pond, and the phenotypic changes were tracked for 20 years. Fish from the last generation were genotyped for the Ectodysplasin-A (Eda) locus, the major gene involved in armour development. We found a strong fitness advantage for the freshwater-type fish (on average, 20% fitness advantage for the freshwater morph, and 92% for the freshwater genotype). The trend is best explained by assuming that this fitness advantage is maximum at the beginning of the invasion and decreases with time. Such fitness differences provide a quantifiable example of rapid selection-driven phenotypic evolution associated with environmental change in a natural population.
Evolution, 2004
Sexual dimorphism is widespread in nature and can be influenced by sex-specific natural selection resulting from ecological differences between the sexes. Here we show that contrasting life-history pressures and temporal shifts in ecology can exert a strong influence on the evolution of sexual dimorphism. The bony spines exhibited by stickleback are a defense against open-water avian predators but may be detrimental against benthic macroinvertebrate predators. Female stickleback from a coastal lake in western Canada occupy a more open-water ecological niche and exhibit greater dorsal and pelvic spine number than males, but the magnitude of these differences varies among lifehistory stages, seasons, and years. Ecological data on diet and parasite load and 62 seasonal estimates of selection over a 15-year period show that selection favors increased spine number in females and decreased spine number in males, but only when pronounced ecological differences between the sexes results in differential exposure to the two, divergent predation regimes. Thus occasional sex-reversals in ecological niche reversed the mode of selection. These processes caused a predictable response in the subsequent generation, indicating that divergent predation caused evolutionary change in dimorphism. However, temporal oscillations in sex-specific selection resulted in no net change in sexual dimorphism over the 15-year study period, indicating that fluctuations in directional selection can be responsible for long-term stasis. Replicated shifts in selective regime can demonstrate the primacy of ecological processes in driving evolution and our results illustrate how such shifts are detectable using long-term monitoring of natural populations.
Current Zoology, 2012
Among-population differences in morphology and behaviors such as boldness have been shown to co-vary with ecological conditions, including predation regime. However, between-and within-population covariation of predator defense morphology with variation in behaviors relevant to ecology and evolution (boldness, exploration, activity, sociability and aggressiveness, often defined as personality traits when they are consistent across time and contexts) have never been quantified together in a single study in juvenile fish from populations found in contrasting environments. We measured predator defense morphology differences between adults from two freshwater populations of threespine sticklebacks with different ecological conditions. We then quantified five behaviors in juveniles from both populations raised in a common environment. Wild-caught adults showed significant differences in predator defense morphology. One population had significantly lower lateral plate number, shorter dorsal spine, pelvic spine and pelvic girdle. Furthermore, 61% of individuals from that population showed an absence of pelvic spine and girdle. At the population level, we found that differences in defense morphology in adults between the two lakes were coupled with differences in behaviors in juveniles raised in a common environment. Levels of activity, aggressiveness and boldness were higher in juveniles from the population lacking predator defense structures. At the individual level, anti-predator morphology of adult females could not predict their offspring's behavior, but juvenile coloration predicted individual boldness in a population-specific manner. Our results suggest that ecological conditions, as reflected in adult predator defense morphology, also affect juvenile behavior in threespine sticklebacks, resulting in trait co-specialization, and that there is a genetic or epigenetic component to these behavioral differences [Current Zoology 58 (1): 53-65, 2012].
Evolutionary Ecology, 2012
The repeated colonization of freshwater habitats by the ancestrally marine threespined stickleback Gasterosteus aculeatus has been associated with many instances of parallel reduction in armour traits, most notably number of lateral plates. The change in predation regime from marine systems, dominated by gape-limited predators such as piscivorous fishes, to freshwater habitats where grappling invertebrate predators such as insect larvae can dominate the predation regime, has been hypothesized as a driving force. Here we experimentally test the hypothesis that stickleback with reduced armour possess a selective advantage in the face of predation by invertebrates, using a natural population of stickleback that is highly polymorphic for armour traits and a common invertebrate predator from the same location. Our results provide no compelling evidence for selection in this particular predator-prey interaction. We suggest that the postulated selective advantage of low armour in the face of invertebrate predation may not be universal.
Ecology and Evolution
While the genetic basis to plate morph evolution of the three-spined stickleback (Gasterosteus aculeatus) is well described, the environmental variables that select for different plate and spine morphs are incompletely understood. Using replicate populations of three-spined sticklebacks on North Uist, Scotland, we previously investigated the role of predation pressure and calcium limitation on the adaptive evolution of stickleback morphology and behavior. While dissolved calcium proved a significant predictor of plate and spine morph, predator abundance did not. Ecol. Evol., xxx, 2014 and xxx performed a comparable analysis to our own to address the same question. They failed to detect a significant effect of dissolved calcium on morphological evolution, but did establish a significant effect of predation; albeit in the opposite direction to their prediction.