Dillon Zoological Studies 2014, 53:31 http://www.zoologicalstudies.com/content/53/1/31 RESEARCH Open Access Cryptic phenotypic plasticity in populations of the North American freshwater gastropod, Pleurocera semicarinata Robert T Dillon Jr Abstract Background: Phenotypic plasticity is termed ‘cryptic’ when it becomes so extreme as to prompt an (erroneous) hypothesis of speciation. Populations of pleurocerid snails nominally identified as Pleurocera (‘Goniobasis’ or ‘Elimia’) livescens are common elements of the macrobenthos in rivers and on lakeshores from Vermont through northern Ohio and northern Indiana to Wisconsin, USA. Small streams in southern Ohio, southern Indiana, and Kentucky are inhabited by Pleurocera semicarinata, and larger rivers by Lithasia obovata. The three nominal species differ only in qualitative aspects of shell morphology - P. semicarinata demonstrating a slender shell with a small body whorl, L. obovata a robust shell with a large body whorl, and P. livescens intermediate. Results: Here I use allozyme electrophoresis to estimate genetic divergence over 11 enzyme loci among three populations of P. livescens, two populations of P. semicarinata, and one population of L. obovata sampled across 650 km of their combined range. With each of these six populations I sample a control population of Pleurocera canaliculata, demonstrating that the genetic divergence among the six known conspecific populations is comparable to that observed among the six study populations. Conclusions: The specific nomina L. obovata and P. livescens would appear to be junior synonyms of P. semicarinata. The shell morphological differences by which these taxa have heretofore been distinguished would appear to result from ecophenotypic plasticity, driven perhaps by predation, substrate, or current. Keywords: Snail; Pleuroceridae; Population genetics; Inducible defenses; Shell morphology; Allozyme electrophoresis; Predation Background and environmental calcium on shell morphology have also In recent years, a great deal of research interest has been been well documented in laboratory populations of basom- directed toward freshwater gastropods as model organisms matophoran snails (Britton and McMahon 2004; Rundle for the study of phenotypic plasticity (e.g., Auld and Relyea et al. 2004; Dillon and Herman 2009). 2011; Brönmark et al. 2012). Most research has focused on Research on phenotypic plasticity in the longer-lived, the basommatophorans, which by virtue of their rapid gen- more slowly growing caenogastropod snails has tended to eration times and ease of culture adapt well to experimen- focus on systematic observations in the field, typically cali- tation. Reared in the presence of crushing predators, brated with independent genetic controls. Dillon (2011) basommatophoran snails tend to develop shells with broad documented a striking tendency for the shells of Pleuro- body whorls (Lakowitz et al. 2008; Brönmark et al. 2011), cera clavaeformis to develop a broader and more ‘robust’ while in the presence of predators extracting snails from morphology as a function of river size in East Tennessee, their apertures, body whorls tend to develop more narrowly suggesting strongly that the shell characters upon which (DeWitt 1998; Langerhans and DeWitt 2002; Hoverman the distinction between the genera Pleurocera, Goniobasis, et al. 2005). The phenotypic effects of temperature, current, and Elimia have been based are attributable to ecopheno- typic plasticity. Dillon et al. (2013) used geometric mor- Correspondence: [email protected] phometrics to document an identical phenomenon in Department of Biology, College of Charleston, Charleston, SC 29424, USA populations of Pleurocera canaliculata sampled in streams © 2014 Dillon; licensee Springer. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. Dillon Zoological Studies 2014, 53:31 Page 2 of 7 http://www.zoologicalstudies.com/content/53/1/31 of varying size from New York to Alabama, USA. Both of may be indistinguishable from juvenile Pleurocera inhabit- these studies involved populations previously assigned to ing small streams nearby (Figure 2). multiple specific nomina by 19th-century taxonomists, Snails bearing shells of a morphology intermediate and both were controlled using genetic similarities calcu- between that of typical P. semicarinata and P. livescens lated over approximately ten polymorphic enzyme loci. are common in natural populations. Thus, workers in Dillon and colleagues coined the term ‘cryptic phenotypic the field have conventionally followed Goodrich (1940), plasticity’ to describe the phenomenon demonstrated by assigning the nomen ‘semicarinata’ to populations in these diverse pleurocerid populations - interpopulation the southern half of the range and the nomen ‘livescens’ morphological variance so extreme as to prompt an (erro- to populations in the north. In Indiana, for example, neous) hypothesis of speciation. Goodrich and van der Schalie (1944) reported the range Thepurposeofthepresentstudyistoextendthefindings of P. livescens to be ‘the Wabash River, the Maumee of Dillon (2011) and Dillon et al. (2013) to include River, and the St. Joseph River of Lake Michigan; prob- freshwater gastropod populations currently identified as ably also in that part of Lake Michigan which borders Pleurocera semicarinata, Pleurocera livescens,andLitha- Indiana.’ They gave the range of P. semicarinata as ‘the sia obovata. ‘Melania’ (now Pleurocera) semicarinata was two forks of the White River, the Whitewater River, the described from ‘Kentucky’ by Thomas Say in 1829, its upper parts of the Big Blue River and probably other range now generally understood to include small streams streams in southern Indiana.’ This division of the state through most of Kentucky, southern Ohio and southern corresponds roughly to the glacial maximum; P. livescens Indiana (Goodrich 1940). ‘Melania’ (now Lithasia) obovata inhabiting the more lentic environments of the north and was also described by Say (1829), just a few paragraphs P. semicarinata the more lotic south. subsequent to his description of M. semicarinata,from Dunithan et al. (2012) sampled 39 populations of Pleuro- ‘Kentucky River,’ and ‘also at the Falls of the Ohio.’ Its cera from Indiana and selected 191 shells varying imper- range is similar to that of P. semicarinata,although ceptibly from those bearing high spires and small body restricted to large rivers (Goodrich 1940). ‘Melania’ (now whorls to those with low spires and broad body whorls. Pleurocera) livescens was described from ‘Lake Erie, New The relative warp axis describing most of this variation York’ by Menke (1830). Populations of P. livescens inhabit was significantly correlated with ten environmental vari- streams, rivers, and lake shores from Wisconsin through ables (of 17 tested), most strongly latitude, longitude, northern Indiana and northern Ohio to Ontario and temperature, flow, conductivity, and substrate. Shells Vermont (Goodrich 1939, 1940; Clarke 1981). sampled from populations in the more lotic lower lati- Pleurocera semicarinata and P. livescens are distin- tudes tended to be more slender. Although Dunithan guishableonlybyqualitative characters of the shell and colleagues identified all 39 of their study populations (Figure 1), populations of the former tending to dem- as P. livescens, the 16 most southern populations they onstrate higher spires, and those of the latter typically sampled would have been identified as P. semicarinata by displaying broader body whorls. L. obovata is more dis- Goodrich and van der Schalie (1944). tinctive, bearing a strikingly robust shell with a much- In the present study, I use allozyme electrophoresis to expanded body whorl, although juvenile L. obovata test the hypothesis that populations historically referred to Pleurocera semicarinata, P. livescens,andLithasia obovata are conspecific, the nomen P. semicarinata (Say 1829) hav- ing priority for the single species represented. Over a span of 30 years, the electrophoretic resolution of allozyme variation has demonstrated great utility as a tool for the measurement of genetic divergence among pleurocerid Figure 1 Example shells from the three nominal species. Left to right: Pleurocera semicarinata from Kentucky population SK, Pleurocera livescens from New York population LN, and Lithasia Figure 2 The shells of four individual L. obovata selected from obovata from Indiana/Kentucky population OF. population OF to show a growth series. Dillon Zoological Studies 2014, 53:31 Page 3 of 7 http://www.zoologicalstudies.com/content/53/1/31 populations throughout eastern North America, with cali- Topotypic population LN of P. livescens and control bration against morphological (Dillon 1984a), chromosomal population AN of P. canaliculata were sampled together (Dillon 1991), and mtDNA sequence divergence (Dillon and near the mouth of Silver Creek, approximately 800 m up- Frankis 2004). The levels of divergence expected both within stream from Lake Erie, the type locality of ‘Melania’ lives- and among conspecific pleurocerid populations have been cens as given by Menke (1830). Study population LM of P. established, and the identification of distinct biological livescens and control population AM of P. canaliculata species is typically unambiguous (Chambers 1980; Dillon were