Post Lab Research: Eco-evo dynamics

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 origins and ecological and evolutionary consequences of intraspecific phenotypic variation in alewives (Alosa pseudoharengus). In eastern North America, there exist two forms of alewives: the ancestral anadromous form that migrates between freshwater lakes and streams and the ocean, and the derived landlocked form that spends its entire life in freshwater lakes. These life history differences have resulted in variation among populations in foraging traits, foraging behavior, habitat used, whole-body morphology, period of residence in freshwater, etc. (Palkovacs and Post 2008; Post et al. 2008; Schielke et al. 2011; Jones et al. 2013). 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 ago (Palkovacs et al. 2008), concurrent with the period of early colonial dam construction in New England (Twining and Post 2013; Twining et al. 2013). 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, Jones et al. 2013). 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; Howeth et al. 2013). 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. Our experimental results 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 2009).

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; Post and Palkovacs 2009). 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. Using historical and contemporary data we have shown that anadromous alewife stocked into Crystal Lake converge on the landlocked phenotype within 50 years (Palkovacs et al. 2014). 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).

The strong effects of alewife on zooplankton has driven evolution in Daphnia ambigua, an important prey for alewife and keystone grazers in lakes. D. ambigua from lakes with anadromous alewife have faster juvenile growth rates, earlier age of maturation, larger clutches, shorter interclutch intervals (all heritable differences), and a greater plastic response in life history traits and sexual reproduction to alewife kairomones than D. ambigua from lakes with landlocked alewife (Walsh and Post 2011, Walsh and Post 2012). The evolution of D. ambigua appear to be caused by selection to reproduce before strong size selective predation by young-of-the-year (YOY) anadromous alewife extirpate daphnia from the water column (typically in late June). As a consequence of this life history evolution, D. ambigua from lakes with anadromous alewife have a greater population growth rate (Walsh and Post 2011), which alters consumer resource dynamics and reduces net primary production in experimental mesocosms (Walsh et al. 2012).

Differences in habitat usage by landlocked and anadromous alewife, and the strong effect of alewife on zooplankton have also caused changes in the growth, habitat distribution and foraging traits of resident fish species. Chain pickerel (the native top predator in our study lakes) is a littoral predator, but in lakes with landlocked alewife a portion of the chain pickerel population has made a novel niche shift towards foraging in pelagic habitats on landlocked alewife (Brodersen et al. 2015). This niche shift is accompanied by greater lipid storage and differences in whole body morphology for the pickerel found foraging offshore. Additionally, bluegill compete with alewife for zooplankton in our study lakes. Bluegill from lakes with landlocked alewife are significantly more efficient at foraging on small-bodied zooplankton than bluegill from lakes with no alewife or anadromous alewife populations (Huss et al. 2014). This is presumably because bluegill from lakes with landlocked alewife only experience small-bodied zooplankton, as a result of the strong effects of alewife on the zooplankton community. Finally, we have found that the growth rates of young-of-the-year largemouth bass is significantly higher in lakes with no alewife (presumably because of the higher biomass and larger body size of zooplankton in those lakes) than lakes with alewife (Boel et al. 2018). Furthermore, YOY bass had higher growth rates in lakes with anadromous alewife populations than in lakes with landlocked alewife populations (Boel et al. 2018).

Related publications (Post Lab publications):

Reid, K., J.C. Garza, S.R. Gephard, A. Caccone, D.M. Post, E.P. Palkovacs. 2020. Restoration mediated secondary contact leads to introgression of alewife ecotypes separated by a colonial-era dam. Evolutionary Applications 13:652-664 doi:10.1111/eva.12890

Beston, S.M., J. L. Dudycha, D.M. Post, and M.R. Walsh. 2019. The evolution of eye size in response to increased fish predation in DaphniaEvolution 73:792-802. doi:10.1111/evo.13717

Boel, M., J. Brodersen, H. Baktoft, A. Koed, and D.M. Post. 2018. Incidence and phenotypic variation in alewife alter the ontogenetic trajectory of young-of-the-year largemouth bass. Oikos 127:1800-1811. doi:10.1111/oik.05556

Brodersen, J., D.M. Post, and O. Seehausen. 2018. Upward Adaptive Radiation Cascades: Predator Diversification Induced by Prey Diversification. Trends in Ecology and Evolution 33:59-70. doi:10.1016/j.tree.2017.09.016

Des Roches, S., D.M. Post, N.E. Turley, J.K. Bailey, A.P. Hendry, M.T. Kinnison, J.A. Schweitzer, E.P. Palkovacs. 2018. Ecological effects of intraspecific variation. Nature Ecology and Evolution 2:57-64doi:10.1038/s41559-017-0402-5

Littrell, K.A., D. Ellis, S.R. Gephard, A.D. MacDonald, E.P. Palkovacs, K. Scranton, and D.M. Post. 2018. Evaluating the potential for pre‐zygotic isolation and hybridization between landlocked and anadromous alewife (Alosa pseudoharengus) following secondary contact. Evolutionary Applications 11:1554-1566 doi:10.1111/eva.12645

Jones, A.W., and D.M. Post. 2016. Does intraspecific competition promote variation? A test via synthesis. Ecology and Evolution 6:1646–1655doi:10.1002/ece3.1991

Walsh, M.R., T. Castoe, J. Holmes, M. Packer, K. Biles, M. Walsh, S. B. Munch, D.M. Post. 2016. Local adaptation in transgenerational responses to predators. Proceedings of the Royal Society B 283:20152271 doi:10.1098/rspb.2015.2271

Brodersen, J., J.G. Howeth, and D.M. Post. 2015. Emergence of a novel prey life history promotes contemporary sympatric diversification in a top predator. Nature Communications 6:8115 doi:10.1038/ncomms9115

Huss, M., J.G. Howeth, J. Osterman, and D.M. Post. 2014. Intraspecific phenotypic variation among alewife populations drives parallel phenotypic shifts in bluegill. Proceedings of the Royal Society B. doi:10.1098/rspb.2014.0275

Palkovacs, E.P., E.G. Mandeville, and D.M. Post. 2014. Contemporary trait change in a classic ecological experiment: rapid decrease in alewife gill-raker spacing following introduction to an inland lake. Freshwater Biology. doi:​10.1111/fwb.12392  

Walsh, M.R., K. J. LaPierre, and D.M. Post. 2014. Phytoplankton composition modifies predator-driven life history evolution in Daphnia. Evolutionary Ecology 28:397-411. doi:10.1007/s10682-013-9666-7

Howeth, J.G., J.J. Weis, J. Brodersen, E.C. Hatton, and D.M. Post. 2013. Intraspecific variation in a fish predator affects multi-trophic lake metacommunity structure. Ecology and Evolution 15:5031-5044. doi: 10.1002/ece3.878

Jones, A.W., E.P. Palkovacs and D.M. Post. 2013. Recent parallel divergence in body shape and diet source of alewife life history forms. Evolutionary Ecology 27:1175-1187doi:10.1007/s10682-013-9650-2

Jones, A.W., and D.M. Post. 2013. Consumer interaction strength may limit the diversifying effect of intraspecific competition: a test in alewife (Alosa pseudoharengus). American Naturalist 181:815-826. doi:10.1086/670197

Twining, C.W., and D.M. Post. 2013. Cladoceran remains reveal presence of a keystone size-selective planktivore. Journal of Paleolimnology 49:253-266. doi:10.1007/s10933-012-9672-8

Twining, C.W., D.C. West, and D.M. Post. 2013. Historical changes in nutrient inputs from humans and anadromous fish in New England’s coastal watersheds. Limnology and Oceanography. 58:1286–1300doi:10.4319/lo.2013.58.4.1286

Weis, J.J., and D.M. Post. 2013. Intraspecific variation in a predator drives cascading variation in primary producer community composition. Oikos. 122:1343–1349. doi:10.1111/j.1600-0706.2012.00258.x

Walsh, M.R., and D.M. Post. 2012. The impact of intraspecific variation in a fish predator on the evolution of phenotypic plasticity and investment in sex in Daphnia ambigua. Journal of Evolutionary Biology 28:80-89.doi:10.1111/j.1420-9101.2011.02403.x

Walsh, M.R., DeLong, J.P., Hanley, T.C., and D.M. Post. 2012. A cascade of evolutionary change alters consumer-resource dynamics and ecosystem function. Proc. R. Soc. B. 279:3184-3192 doi:10.1098/rspb.2012.0496

Walsh, M.R., and D.M. Post. 2011. Interpopulation variation in a fish predator drives evolutionary divergence in prey in lakes. Proc. R. Soc. B. 278:2628-2637. doi:10.1098/rspb.2010.2634

Jones, A.W., C.M. Dalton, E.S. Stowe, and D.M. Post. 2010. Contribution of declining anadromous fishes to the reproductive investment of a common piscivorous seabird, the double-crested cormorant (Phalacrocorax auritus).Auk 127:696-703. doi:10.1525/auk.2010.09200

West, D.C., A.W. Walters, S. Gephard, and D.M. Post. 2010. Nutrient loading by anadromous alewives (Alosa pseudoharengus): contemporary patterns and predictions for restoration efforts. Canadian Journal of Fisheries and Aquatic Sciences 67:1211-1220. doi:10.1139/F10-059

Dalton, C.M., D. Ellis, and D.M. Post. 2009. The impact of double-crested cormorant (Phalacrocorax auritus) predation on anadromous alewife (Alosa pseudoharengus) in south-central Connecticut, USA. Canadian Journal of Fisheries and Aquatic Sciences 66(2): 177–186. doi:10.1139/F08-198

Palkovacs, E.P., and D.M. Post. 2009. Experimental evidence that phenotypic divergence in predators drive community divergence in prey. Ecology 90(2): 300-305. doi:10.1890/08-1673.1

Post, D.M., and E.P. Paklovacs. 2009. Eco-evolutionary feedbacks in community and ecosystem ecology: interactions between the ecological theater and the evolutionary play. Philosophical Transactions of the Royal Society B 364: 1629-1640. doi:10.1098/rstb.2009.0012

Post, D.M. and A.W. Walters. 2009. Nutrient excretion rates of anadromous alewives during their spawning migration. Transactions of the American Fishery Society 138(2): 264–268. doi:10.1577/T08-111.1

Walters, A.W., R.T. Barnes, and D.M. Post. 2009. Anadromous alewives (Alosa pseudoharengus) contribute marine-derived nutrients to coastal stream food webs. Canadian Journal of Fisheries and Aquatic Sciences 66(3): 439–448. doi:10.1139/F09-008

Palkovacs, E.P., K.B. Dion, D.M. Post, and A. Caccone. 2008. Independent evolution of landlocked alewife populations and rapid, parallel evolution of phenotypic traits. Molecular Ecology 17:582-597.

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 10:699-720.

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.