Eco-evolutionary feedbacks - ecological and evolutionary implications of intraspecific variation
Variation in traits within a species (intraspecific phenotypic variation) likely has important implications for species interactions, ecosystem dynamics and the dynamic feedback between ecology and evolution. Since 2004, the Post Lab has been studying the ecological and evolutionary consequences of intraspecific phenotypic variation in alewives (Alosa pseudoharengus). In eastern North America, there exist two forms of alewives: a landlocked form that spends its entire life in freshwater lakes and an anadromous form that migrates between freshwater lakes and the ocean. These life history differences have resulted in variation among populations in foraging traits, foraging behavior, period of residence in freshwater, etc. While some of the landlocked populations in Connecticut were stocked from previously landlocked populations, many derive directly from anadromous ancestors (Palkovacs et al. 2008). Population genetics indicate that most of the "naturally" landlocked alewife populations (populations that were not stocked) were isolated from their anadromous ancestors 250-500 years before present - concurrent with the period of early colonial dam construction in New England. Our results suggest morphological differences are independently evolved and that rapid parallel evolution has shaped the foraging traits of landlocked alewives.
Landlocked alewives are famous for their role in structuring pelagic zooplankton communities (Brooks and Dodson 1965). They are well studied throughout the Laurentian Great Lakes region because, as an invasive species, they have had large impacts on food web structure and ecosystem processes. In comparison, much less is known about the ecological role of anadromous alewives. Landlocked and anadromous alewives differ in the time they spend in freshwater (year round for landlocked, seasonal for anadromous), morphological traits related to foraging, and their size selectivity of prey (Palkovacs and Post 2008). Anadromous alewives have feeding morphology better adapted to feeding on large-bodied prey while landlocked alewives have feeding morphology better adapted to feeding on small-bodied prey. Using a whole-lake comparative study, we have shown that the phenotypic differences dramatically alter the direct effects of alewife predation on zooplankton communities and the strength of cascading trophic interactions caused by alewives (Post et al. 2008). Our results are among the first to demonstrate that intraspecific phenotypic variation in a predator can alter the form and strength of complex trophic interactions.
We have further tested the results from whole lake comparative studies in small-scale mesocosm experiments. The small-scale experiments allow us to isolate the effects of morphological differences from the potential influence of seasonality, density, and the influence of other species. We have found in the small-scale experiments results that are nearly identical to those found at the whole-lake scale. Differences between landlocked and anadromous alewives in feeding morphology and diet selectivity drive differences in zooplankton community structure (Palkovacs and Post in review).
The origin of intraspecific phenotypic variation among alewife populations has important implications for our understanding of dynamics at the interface of ecology and evolution (eco-evolutionary dynamics). The Post Lab has shown that a change in alewife migratory habit has strengthened the nature of eco-evolutionary feedbacks and led to ecological and evolutionary divergence between anadromous and landlocked alewife systems (Palkovacs and Post 2008). In lakes with landlocked alewives, intense predation permanently eliminates large prey items from the environment, placing landlocked populations under strong selection for foraging on small-bodied zooplankton prey. This strong selection has favored a foraging morphology adapted to feeling on small-bodied zooplankton. In contrast, anadromous alewives encounter large-bodied zooplankton each spring. When anadromous alewives eliminate these large prey items from the freshwater environment, the alewives emigrate to the marine environment where they, again, encounter and feed on large zooplankton. This switch from the freshwater to the marine environment, coupled with the annual recovery of large-bodied zooplankton in lakes with anadromous alewives, appears to maintain selection on anadromous alewife foraging traits that facilitates the capture of large prey items. Thus, the eco-evolutionary feedbacks are very strong in lakes with landlocked alewives and weak in lakes with anadromous alewives. This research shows for the first time that spatial variation in the strength of eco-evolutionary interactions can be an important engine shaping patterns of ecological diversity (e.g. community structure) and evolutionary diversity (e.g. phenotypic variation) in nature. Small scale experiments, used to isolate the role of morphological differences, have shown that the effects observed at the whole lake scale are a results of differences in feeding morphology (Palkovacs and Post 2008). These results are among the first demonstrations that intraspecific phenotypic variation in a predator can alter the form and strength of complex trophic interactions.
One of the more striking differences between young-of-the-year anadromous and landlocked alewives is their diet selectivity (Palkovacs and Post 2008). Once they reach 25-30 mm in length (when gape is no longer limiting), anadromous alewives prey upon the very largest zooplankton in the lake. This is Daphnia spp. for about 2 weeks in June before they are extirpated, and then large predatory copepods for most of the summer (Mesocyclops edax and the omnivorous Tropocyclops extensus) until they are extirpated. In contrast, landlocked alewives prey upon small-bodied herbivorous zooplankton (i.e., Bosmina and calanoid copepods) throughout the year. Differences in diet are consistent with observed morphological differences and are made possible by differences in the seasonal dynamics of zooplankton between anadromous and landlocked lakes. In anadromous lakes, large-bodied zooplankton are able to re-establish over the winter and by early spring provide high densities of large-bodied prey for the new cohort of anadromous alewives. This allows anadromous alewives to prey upon large, predatory zooplankton for a substantial period of the summer. In contrast, landlocked alewives prey upon small herbivorous zooplankton throughout the year. Preliminary diet and stable isotope analyses suggest that the trophic position of anadromous alewives diverges from that for landlocked alewives in August, but then converges again once the large, predatory copepods are eliminated from the lake. The trophic divergence is around 0.5 trophic levels. Our findings suggest that divergence in zooplankton community structure, caused by divergent predation by alewives, feeds back to influence prey availability and prey selectivity, which results in trophic differentiation between landlocked and anadromous alewives.
The effects of alewives on zooplankton community structure is likely to propagate through the lake food webs in which they reside. We are currently testing the effects of alewives on largemouth bass and bluegill foraging behavior, trophic position and morphology. In future years we plan to test how changes in bluegill foraging behavior and morphology - which we believe have responded to changes in the zooplankton community caused by alewife predation - influences their role in the food webs of our study lakes. We are also interested in the evolutionary response of zooplankton prey to the incidence of and phenotypic variation among alewife population.
Our research on alewives has important implications to the management of coastal lakes and to the conservation and management of anadromous alewives, which are a federally listed species of concern. The Post Lab is active in local river restoration efforts and has a close working relationship with the CT DEP diadromous fish program. A fish counter installed at the Branford Supply Ponds fishway has provided real time information about the recovery of alewives in the the Branford Supply Ponds and the Linsley Pond watershed where the Post lab is testing the effects of restoration on coastal lake ecosystems. The Branford Supply Ponds Fishway received a Coastal American Partnership Award in 2006.
For more information and updates on results from this research project please see the Landlocked and Anadromous Alewife Research Project (LAARP) web site.
Related publications (Publications):
Dalton, C.M., D. Ellis, D.M. Post. In review. The impact of Double-crested Cormorant predation on anadromous alewives in south-central Connecticut. Canadian Journal of Fisheries and Aquatic Sciences
Post, D.M., E.P. Palkovacs, E.G. Schielke, and S.I. Dodson. 2008. Intraspecific phenotypic variation in a predator affects zooplankton community structure and cascading trophic interactions. Ecology 89: 2019-2032
Palkovacs, E.P., and D.M. Post. 2008. Eco-evolutionary interactions between predators and prey: can predator-induced changes to prey communities feedback to shape predator foraging traits? Evolutionary Ecology Research. In press.
Palkovacs, E.P., K.B. Dion, D.M. Post, and A. Caccone. 2008. Independent evolutionary origin of landlocked alewife populations and rapid parallel evolution of phenotypic traits. Molecular Ecology 17:582-597.