Contemporary and historical evolutionary processes interact to shape patterns of within‐lake phenotypic divergences in polyphenic pumpkinseed sunfish,Lepomis gibbosus

Abstract

Historical and contemporary evolutionary processes can both contribute to patterns of phenotypic variation among populations of a species. Recent studies are revealing how interactions between historical and contemporary processes better explain observed patterns of phenotypic divergence than either process alone. Here, we investigate the roles of evolutionary history and adaptation to current environmental conditions in structuring phenotypic variation among polyphenic populations of sunfish inhabiting 12 postglacial lakes in eastern North America. The pumpkinseed sunfish polyphenism includes sympatric ecomorphs specialized for littoral or pelagic lake habitats. First, we use population genetic methods to test the evolutionary independence of within-lake phenotypic divergences of ecomorphs and to describe patterns of genetic structure among lake populations that clustered into three geographical groupings. We then used multivariate analysis of covariance (MANCOVA) to partition body shape variation (quantified with geometric morphometrics) among the effects of evolutionary history (reflecting phenotypic variation among genetic clusters), the shared phenotypic response of all populations to alternate habitats within lakes (reflecting adaptation to contemporary conditions), and unique phenotypic responses to habitats within lakes nested within genetic clusters. All effects had a significant influence on body form, but the effects of history and the interaction between history and contemporary habitat were larger than contemporary processes in structuring phenotypic variation. This highlights how divergence can be better understood against a known backdrop of evolutionary history.

Dissecting a potential spandrel of adaptive radiation: Body depth and pectoral fin ecomorphology coevolve in Lake Malawi cichlid fishes

“…Both body depth and pectoral fin morphology could commonly influence critical aspects of organismal diversification such as habitat specialization (Geerlink, 1983;Gerstner, 1999;Fulton et al, 2001;Higham, 2007aHigham, , 2007bTobler et al 2008;Weese et al, 2012;Hulsey et al, 2013;Colombo et al, 2016), trophic convergence (Collar, Wainwright, & Alfaro, 2008;Krabbenhoft et al, 2009;Ruber & Adams, 2001;Rupp & Hulsey, 2014), and speciation (Elmer et al, 2010;Hendry & Taylor, 2004;Husemann et al, 2017;Pfaender et al, 2010). What also seems likely is that each trait individually influences a number of both independent and correlated behaviors across species that link morphology to species interactions (Brönmark & Miner, 1992;Bakker & Mundwiler, 1999;Hechter, Moodie, & Moodie, 2000;Wainwright et al, 2002;Pigliucci, 2003;Domenici et al, 2008;Blob et al 2010;Monteiro & Nogueira, 2010;Head et al, 2013;Price et al, 2015).…”

Does phenotypic plasticity initiate developmental bias?

“…We suggest that bias in plasticity could be inferred from patterns in two main ways: (a) As similar responses to the same environmental cues across lineages and populations, or (b) as similar responses to dissimilar environmental cues if biases are more extreme. For pumpkinseed, these polymorphisms are known to occur repeatedly across several populations in Ontario, Canada, as well as in the Adirondacks of New York State, which respectively form two lineages (Weese, Ferguson, & Robinson, 2012). For example, in centrarchid fishes, resource polymorphisms are known to exist in both pumpkinseed and bluegill sunfish whereby individuals within a single lake adaptively diverge into specialists that focus on either benthic or limnetic habitats with corresponding changes in head and body shape (Ehlinger & Wilson, 1988;Robinson, Wilson, Margosian, & Lotito, 1993).…”

“…It is commonly appreciated that a wide range of species will often show similar responses to the same environmental cues (Robinson & Parsons, 2002;Martinez-Garcia et al, 2014). Experiments show that pumpkinseeds from different lakes and ancestral lineages respond in a similar way to benthic and limnetic diet treatments (Parsons & Robinson, 2006, 2007Robinson & Wilson, 1996;Weese et al, 2012). For pumpkinseed, these polymorphisms are known to occur repeatedly across several populations in Ontario, Canada, as well as in the Adirondacks of New York State, which respectively form two lineages (Weese, Ferguson, & Robinson, 2012).…”

“…For example, in centrarchid fishes, resource polymorphisms are known to exist in both pumpkinseed and bluegill sunfish whereby individuals within a single lake adaptively diverge into specialists that focus on either benthic or limnetic habitats with corresponding changes in head and body shape (Ehlinger & Wilson, 1988;Robinson, Wilson, Margosian, & Lotito, 1993). For pumpkinseed, these polymorphisms are known to occur repeatedly across several populations in Ontario, Canada, as well as in the Adirondacks of New York State, which respectively form two lineages (Weese, Ferguson, & Robinson, 2012). Experiments show that pumpkinseeds from different lakes and ancestral lineages respond in a similar way to benthic and limnetic diet treatments (Parsons & Robinson, 2006, 2007Robinson & Wilson, 1996;Weese et al, 2012).…”

Assortative mating but no evidence of genetic divergence in a species characterized by a trophic polymorphism

“…Indeed, foraging ecomorphs have been identified in populations of bluegill in Michigan (USA) and Japan when pumpkinseed are absent (Ehlinger & Wilson, ; Ehlinger, ; Yonekura et al ., ). For pumpkinseed, almost 30 lakes with foraging ecomorphs have been reported in the Canadian Shield (Ontario, Canada) and Adirondack (New York, USA) regions, consistently in the absence of bluegill (Robinson et al ., ; Jastrebski & Robinson, ; Weese et al ., ).…”