Dr. Rob Dillon, Coordinator





Friday, July 11, 2014

Elimia livescens and Lithasia obovata are Pleurocera semicarinata

Faithful readers of this blog will by now be familiar with cryptic phenotypic plasticity in the shell morphology of pleurocerid snails – interpopulation variance so extreme as to prompt an (erroneous) hypothesis of speciation.  We first documented the phenomenon in our (2011) survey of Pleurocera clavaeformis in East Tennessee [1] under the term “Goodrichian taxon shift,” and generalized the concept to “cryptic phenotypic plasticity” in our (2013) study of Pleurocera canaliculata ranging from New York through the Midwest to North Alabama [2].

Now in a third installment of the series, published in this month’s issue of Zoological Studies [3], we document what may be the most surprising example of the phenomenon yet brought to light.  And again, it might be easiest to understand the significance of the discovery if we back up to the 19th century and take a running start at it.

Thomas Say described “Melania semicarinata” from “Kentucky” in 1829, one year before C. T. Menke described his “Melania livescens” from “Lake Erie, New York.”  Classically, livescens populations bear short, stubby shells while the shells of semicarinata are more slender.  But the populations inhabiting most of the Midwest seem to vary tremendously in shell morphology, such that the distinction between semicarinata and livescens simply disappears.  Calvin Goodrich (1940) divided the species ranges roughly at the glacial maximum, giving the range of semicarinata as “tributaries of Ohio River, Scioto River, Ohio, to Big Blue River, Indiana; Licking River to Salt River in Kentucky; two creeks of Green River of Kentucky” and that of livescens as “tributaries of Ohio River, east of Scioto River in Ohio; Wabash River and branches, west to Illinois River.  Especially common in the St. Lawrence basin.” [4]

But one gets the impression that this division was rather arbitrary on Goodrich’s part.  Our colleagues Steve Jacquemin and Mark Pyron published a nice morphometrics paper back in 2012 [5] showing that Indiana populations bearing broader shells tend to be found in more lentic environments at higher latitudes, and that populations bearing slender shells tend to be found in lotic waters at lower latitudes.  Our Indiana friends identified all 39 of their study populations as “Elimia livescens,” but Goodrich would have identified the 16 populations they sampled from the southern half of the Hoosier State as Goniobasis semicarinata.

I began thinking about a test of the hypothesis that semicarinata and livescens populations might be conspecific in the spring of 2009.  And it was obvious to me that if I were to use the genetic tools that have stood me in such good stead for 30 years, I would need some sort of external calibration.  The combined range of nominal livescens and semicarinata together would extend across 12 states and two Canadian provinces, much larger than any area I had heretofore surveyed.  How much genetic divergence might one expect among conspecific pleurocerid populations spread across so large a region?

So (again, this was back in 2009) it occurred to me that populations of (what I called at the time) Pleurocera acuta also range from New York through the Midwest to Kentucky, and that nobody has ever questioned their conspecific status.  So along with each study population of either semicarinata or livescens, I resolved to sample a control population of Pleurocera acuta.  And if the genetic divergence among my semicarinata/livescens study populations proved no greater than that of my acuta controls, the evidence would suggest that livescens (Menke 1830) is a junior synonym of semicarinata (Say 1829).  I actually made several field trips through Kentucky, Ohio, and Indiana in the summer of 2009, sampling pleurocerid populations under this original (much simpler) study design.

At this point in my narrative, any of my readership who might be pathologically curious about the process of scientific discovery in your particularly feeble-minded correspondent might insert the essay I wrote last year regarding Pleurocera acuta, P. canaliculata, and P. pyrenellum [6].  It was only in the summer of 2010, after I had already begun work on my semicarinata/livescens project, planning to use acuta as a control, that it dawned on me that the situation with canaliculata/acuta might be as big a mess as semicarinata/livescens [7].  And since I couldn’t interpret my semicarinata/livescens data without a canaliculata/acuta calibration, the canaliculata/acuta problem had to be solved and published first.

And that’s how I stumbled upon the headline news – the relationship of semicarinata/livescens to Lithasia obovata.  Sampling the main Ohio River at the type locality for Pleurocera canaliculata in August of 2011, I encountered the first population of L. obovata I had ever personally examined on the hoof.
The hypothesis that populations which Thomas Say described as “Melania obovata” from the Kentucky River back in 1829 might be a startlingly robust, big-river morph of semicarinata/livescens did not immediately dawn on me, however.  True, juvenile obovata do look a bit like Goniobasis or Elimia, which are the genera to which semicarinata and livescens have historically been assigned. 

And indeed, in 1934 Calvin Goodrich documented the same upstream-downstream relationship between the slender, lightly-shelled “sordida form” of L. obovata and more typical, heavily-shelled “forms” in the Green River of Kentucky that he documented between the slender, lightly-shelled pinguis form of Lithasia geniculata and more typical, heavily-shelled forms in the Duck River of Tennessee [8].  It was Goodrich’s 1934 analysis of shell morphological intergradation in the L. geniculata populations of the Duck River that prompted me to coin the term “Goodrichian Taxon Shift” in his honor in 2007 [1].  And sordida (Lea 1841) was initially assigned to the genus Goniobasis by Tryon, just as pinguis (Lea 1852) was initially assigned to Anculosa.

Was Goodrich’s (1934) Plate 1 riding around in the back of my mind in 2011?  [Click the thumbnail below for a larger version.]  Figures 1 – 9 and 12 depict what Goodrich considered “forms” of Lithasia obovata, including figures 2, 6, and 12, which are all obviously Pleurocera semicarinata.  Figures 10, 11, and 14 depict his “forms” of Lithasia geniculata (Figure 11 is pinguis), which I first extracted and figured way back in 2007 as an illustration of Goodrichian taxon shift.

In the end, I’m not sure what led me to include a sample of 32 Lithasia obovata in a two-phase study already groaning with five populations of nominal acuta, four populations of canaliculata, three populations of semicarinata, three populations of nominal livescens, and a population of nominal pyrenellum from North Alabama thrown in for good measure.  But I’m glad that I did.

I have always considered myself philosophically conservative, in the sense that my initial reaction to change of any sort is negative.  And I am very sensitive to the unhappy side-effects of the taxonomic changes that I have proposed for the North American Pleuroceridae in recent years, especially with regard to the indexing function.  The best general work on the biology of the creatures to which I have dedicated my career is the 1965 paper by B. C. Dazo, “The morphology and natural history of Pleurocera acuta and Goniobasis livescens [9].”  With the publication of my most recent paper, Dazo’s study populations have now become Pleurocera canaliculata and Pleurocera semicarinata, nearly impossible to retrieve by a simple electronic search.

So let’s use subspecies, shall we?  The FWGNA Project has adopted the standard definition of the term “subspecies” as it has been understood since the birth of the Modern Synthesis: “populations of the same species in different geographic locations, with one or more distinguishing traits” [10].  Clearly some populations of Pleurocera semicarinata inhabiting big rivers bear shells so robust as to warrant distinction as P. semicarinata obovata, and other populations in more northern latitudes bear broader shells distinguishable as P. semicarinata livescens.  Such a system will preserve the indexing function of the old names, without compromising our growing storehouse of new evolutionary insights to the ever-surprising freshwater gastropods of North America.

Notes

[1] Dillon, R. T., Jr. (2011)  Robust shell phenotype is a local response to stream size in the genus Pleurocera.  Malacologia 53: 265-277.  [pdf]  For more, see:
  • Goodrichian Taxon Shift [20Feb07]
  • Mobile Basin III: Pleurocera puzzles [12Oct09]
  • Goodbye Goniobasis, Farewell Elimia [23Mar11]
[2] Dillon, R. T., Jr., S. J. Jacquemin & M. Pyron (2013) Cryptic phenotypic plasticity in populations of the freshwater prosobranch snail, Pleurocera canaliculata.  Hydrobiologia 709: 117-127. [html] [pdf]  For more, see:
  • Pleurocera acuta is Pleurocera canaliculata [3June13]
[3] Dillon, R. T., Jr.  (2014) Cryptic phenotypic plasticity in populations of the North American freshwater gasgtropod, Pleurocera semicarinata.  Zoological Studies 53:31. [html] [pdf]

[4] Goodrich, C. (1940) The Pleuroceridae of the Ohio River system.  Occas. Pprs. Mus. Zool. Univ. Mich. 417: 1-21.

[5] Dunithan, A., S. Jacquemin & M. Pyron (2012)  Morphology of Elimia livescens (Mollusca: Pleuroceridae) in Indiana, USA, covaries with environmental variation.  Am. Malac. Bull. 30: 127 – 133.

[6] Pleurocera canaliculata and the process of scientific discovery [18June13]

[7] And now you know the rest of the story.  In my essay of 18June13 (link above) I wrote, "Standing knee-deep in Savannah Creek (maybe 20 km N of Chattanooga) on that memorable day, it suddenly struck me that the snails crawling around my feet might be Pleurocera acuta."  This revelation was only possible because I had spent several weeks that previous summer travelling around the Midwest hunting Pleurocera acuta.  In retrospect, I think the only way I was able to make the acuta/canaliculata/pyrenellum connection in 2010 was that by that time I had personal field experience across the entire 12-state range of the species, from Yankeeland to Dixie.  This is something that Thomas Say, or George Tryon, or even Calvin Goodrich, could never have contemplated.  Good day.

[8] Goodrich, C. (1934) Studies of the gastropod family Pleuroceridae – I.  Occas. Pprs. Mus. Zool. Univ. Mich. 286: 1-17.

[9] Dazo, B.C. (1965) The morphology and natural history of Pleurocera acuta and Goniobasis livescens (Gastropoda: Cerithiacea: Pleuroceridae). Malacologia 3:1-80.

[10] For a complete review of FWGNA policies on the taxonomic level of the subspecies, see:
  • What is a subspecies? [4Feb14]
  • What subspecies are not [5Mar14]

14 comments:

  1. What do common garden experiments show? Do the upstream variants and downstream variants converge morphologically when raised in identical environments?

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    1. They would show that juveniles share the morphology of their parents. There's a reason Dillon has never done such an experiment.

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    2. Good question, Chris. Although common garden experiments are rather routinely published in the freshwater pulmonate literature, they remain quite rare for prosobranchs. Pleurocerids (in particular) are just not good lab animals - relatively long generation times, low fecundities, sort-of a pain. The only study of which I am aware is by Urabe (1998) showing essentially zero heritability for shell shape in Japanese Semisulcospira. So the bottom line is that the field is wide open. Go for it!

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    3. It would be very interesting to figure out what signal (predator kairomones, flow, substrate, etc.) is inducing this pattern. A simple and elegant experiment could be set up to figure this all out, assuming you could keep them alive in culture. I myself have had very modest luck keeping Pleurocerids alive and breeding in captivity.

      -Matt Hill

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    4. What about Whelan et al 2012 in Journal of Molluscan studies? That did a common garden experiment on a leptoxis species and found a strong genetic component for intraspecific shell variation and no evidence of phenotypic plasticity. Surely Rob had heard of this study.

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    5. Actually, the Whelan et al (2012) study is about shell carination, not shell shape per se. Reading Whelan's paper a couple years ago, my thought was that his carinate "Leptoxis ampla" might actually be a Cahaba population of Leptoxis taeniata, conventionally considered endemic to the Black Warrior drainage next door. I'm sure Whelan has read Dillon & Lydeard (1998), so this hypothesis must have occurred to him. But why he didn't mention it in his 2012 paper, or cite Dillon & Lydeard for that matter, is an open question.

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    6. Leptoxis taeniata was never considered to be in the Black Warrior drainage, at least not by anyone who knew what they were taking about. Plus, there's no record of a carinate form of L. taeniata.

      Trying to say shell carination isn't part of shell shape is awful nit picky especially considering some of your previous clams of ecophenotypic plasticity included carinate shell forms.

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  2. Another awful paper from an awful scientist. How can allozymes and cord distances possibly be used to test that shell shape is a response to environment? Surely allozyme loci have nothing to do with shell shape so how can it be claimed that the same genotype is giving rise to different phenotypes (that's the definition of ecophenotypic plasticity)?

    Perhaps you're using methods 30 years old because modern tools would not support your wild hypotheses.

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  3. How many times was this rejected before you finally found a journal that got reviewers who didn't know anything about the topic and recommended this for publication?

    -an anonymous reviewer who rejected this paper in a different journal

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  4. I look at your figure 4 in your paper and see something entirely different. I see 1) true E. livescens (IN, MI & NY), 2) true L. obovata, true E. semicarinata (OH & KY), 3) true P. canaliculata (KY, OH, fall, IN), 4) what we'll call true P. acuta (=canaliculata NY & MI); after all, canaliculata isn't really from NY and MI), and 5) a misidentified pleurocerid of some kind because semicarinata isn't in Virginia, but is found in small, direct Ohio River tribs (in OH, KY, IN, and IL).

    My list matches what Burch (1989) and Johnson et al. (2013) reported. Why can't see your tree for what it is and what the general scientific community accepts? Can you twist the data to show all pleurocerids are Melania ('Goniobasis’ or ‘Elimia’) canaliculata? That would make my life simpler, especially when dealing with conservation issues.

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    1. Sorry complicate your life! But please do review my 2013 paper with Jacquemin and Pyron. In that work we used an upstream/downstream approach to confirm that canaliculata = acuta = pyrenellum. So since the levels of divergence among semicarinata, livescens, and obovata populations are comparable to canaliculata, acuta, and pyrenellum... connect the dots. Your inference (5) is a good one, however. I'm beginning to doubt that those semicarinata-like pleurocerid populations in the Great Valley of Virginia are actually semicarinata myself.

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    2. Thanks Rob. Your paper with Jacquemin and Pyron is interesting, but not being 100% convinced means I would be connecting the dots on adjoining pages. By connecting the dots, you are saying E. livescens = P. acuta, which is not at all true. They are clearly two different species.

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  5. Eek. Let's back up and get a running start at this. Last year Stephen Jacquemin, Mark Pyron and I showed that Pleurocera acuta is conspecific with P. canaliculata. So in my 2014 paper, I sampled a control population of canaliculata/acuta with each study population of semicarinata, livescens, or obovata. Figure 4 shows that the minimum genetic similarity among my six study populations was I = 0.633, comparable to the minimum similarity of I = 0.661 for the controls. Thus semicarinata, livescens & obovata are as conspecific as canaliculata & acuta. This analytical approach is called "calibration.: We "calibrated" the observed divergence among our study populations with known divergence among controls.

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    1. I think the problem with this approach is that the calibration isn't biologically meaningful to begin with and the logic is circular. You could probably pick any three pleurocerids and get the same answer. Does that mean we should just start synonymizing snails in triplicate?

      Allozymes are also known to have problems with convergence which could give such values. Not to mention they were designed for population level studies, and if the null hypothesis is that you're dealing with three species them allozymes are an inappropriate tool for such a study.

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