Dr. Rob Dillon, Coordinator





Thursday, June 2, 2016

The Shape-shifting Pleurocera of North Alabama


The Tennessee River south of Chattanooga reminds me of Danica Patrick on three tires.  Swerving wildly out of the fertile Valley & Ridge Province of East Tennessee, she slices through the Cumberland Plateau at Walden Ridge, bounces off the NW Georgia guard rail, and plunges into the Interior Plains of North Alabama.  The character of the freshwater gastropod fauna changes slightly but perceptibly – not so much in the main river as in the tributaries.  The little black Pleurocera simplex populations, so common in springs and small streams of East Tennessee, disappear west of Chattanooga, to be replaced by populations of the larger and more impressively-shelled P. laqueata.

The most conspicuous element of the Tennessee River macrobenthos through this entire region is Pleurocera canaliculata (Say, 1821) bearing shells of the typical, robust form.  The smaller tributaries are inhabited by a more slender and lightly-shelled ecophenotypic variant, originally described by T. A. Conrad in 1834 as “Melania pyrenellum.”  In 2013 Stephen Jacquemin, Mark Pyron and I presented evidence that the distinction between Conrad’s pyrenellum in small tributaries and Say’s canaliculata in the main Tennessee River is “cryptic phenotypic plasticity,” intrapopulation morphological variance so extreme as to prompt an (erroneous) hypothesis of speciation [1]

Fig 1. Typical Pleurocera canaliculata from the Tennessee R at Site #1.
The sample of typical P. canaliculata canaliculata depicted in Figure 1 above was collected from the Tennessee River at Decatur, Alabama – marked as site #1 on the map below [2].  Stephen, Mark, and I showed that this population is conspecific with the population of P.canaliculata pyrenellum depicted in Figure 2 below, collected from Limestone Creek at Site #2.  I reviewed the evolutionary biology of P. canaliculata throughout eastern North America generally in a pair of related essays posted on this blog back in June of 2013 [3].

Fig 2.  Pleurocera canaliculata pyrenellum from Limestone Creek at Site #2.
The situation is similar in the case of P. clavaeformis, another notorious shape-shifter.  Pleurocera clavaeformis is the most common freshwater gastropod in East Tennessee, ranging from small creeks into large rivers, although not inhabiting the main Tennessee River itself.  Populations of clavaeformis bearing more robust shells in the larger rivers were for many years identified (erroneously) as the distinct species Pleurocera unciale and P. curtum [4].  I first documented cryptic phenotypic plasticity in East Tennessee populations of P. clavaeformis in February of 2007, returning to the subject again in October 2009 and March 2011 [5].

Fig 3.  The Tennessee River west of Knoxville.
Populations of P. clavaeformis are common in several of the Tennessee tributaries of North Alabama, including the Elk, Flint, and Paint Rock Rivers.  These populations generally seem to bear robust shells, however, and have historically been identified as “Pleurocera curtum.”  Goodrich, in fact, stated that Pleurocera (Goniobasis) clavaeformis “does not make the westward turn around Walden Ridge” because he was unaware of any North Alabama populations bearing shells of the lighter, more typical form inhabiting streams of the Cumberland Plateau or Interior Plains [6].

I myself cannot boast of extensive field experience in the state of Alabama.  But I collected the mixed sample of P. clavaeformis and P. canaliculata shown in Figure 4 below from the Paint Rock River SE of Huntsville in March of 1988 (marked as Site #4 above).  The shell variation was rather dramatic in the P. clavaeformis population (top row), ranging from medium-typical to robust-curtum.  The P. canaliculata population (bottom row) was more uniformly heavy-shelled, ranging only from skinnyish-typical to plain-vanilla-typical.

Fig 4.  Pleurocera clavaeformis and P. canaliculata from the Paint Rock at Site 4.
Most significantly, notice that my 1988 sample of Pleurocera from the Paint Rock River did not include any shells demonstrating the pyrenellum morphology, as depicted in Figure 2.  Phenotypic plasticity manifests itself most cryptically where small streams like Limestone Creek empty directly into large rivers, like the Tennessee.  In such situations, the population bearing the more gracile shell morphology will differ strikingly from the population bearing the robust shell, sometimes even mixing unconformably at the mouth of the creek, looking like reproductively-isolated biological species.  But in rivers that grow larger gradually, such as the Paint Rock, the shell morphology of the pleurocerid population changes gradually, and taxonomists are usually not fooled.

It is perhaps for this reason that Goodrich [6] did not report Pleurocera of the pyrenellum form from the Paint Rock River drainage, or indeed from any of the larger tributaries of the Tennessee in North Alabama, such as the Flint or the Elk.  Goodrich gave the distribution of pyrenellum as “tributaries of the Tennessee River in Morgan and Limestone Counties” downstream from the Paint Rock, “and Walker County, Georgia” upstream from the Paint Rock, but not in Madison or Jackson Counties, through which the Paint Rock River runs.  The canaliculata population of the Paint Rock subdrainage just looks like typical canaliculata.  It doesn’t fool anybody.

So for the last three months, we’ve been studying (in excruciating detail) the recent paper by Nathan Whelan and Ellen Strong on mtDNA sequence divergence among the pleurocerid populations of North Alabama [7].  Previously our attention has focused on populations of Leptoxis [8].  But Whelan & Strong also sampled five populations they identified as “Pleurocera prasinata” from tributaries of the Cahaba River draining south through Alabama into the Mobile Basin, and one population they identified as “Pleurocera pyrenellum” from a tributary of the Paint Rock River in Jackson County [9].  That Paint Rock tributary site is marked as Site A on the map above.

Whelan & Strong's Fig 7.  Row C shows putative "Pleurocera pyrenella."  
Whelan & Strong’s Figure 7 is reproduced above, showing example shells from their sample of “Pleurocera pyrenellum” on Row C, at the bottom.  These specimens do not look like the pyrenellum form of P. canaliculata to me.  The shells borne by pyrenellum are flat-sided, almost trapezoidal, essentially demonstrating no suture or indeed any whorl, as shown in Figure 2.  North Alabama pyrenellum populations also typically bear shells marked with spiral cords, especially around the aperture.  But the shells depicted in Row C of Whelan & Strong’s figure seem to lack spiral cords, and demonstrate the slightly rounded whorls and impressed sutures typical of Pleurocera clavaeformis

I hasten to stipulate that I have no personal observations from the Paint Rock subdrainage as far upstream as the Whelan & Strong sample.  And of course, the entire theme of the present essay has been one of caution regarding the use of shell morphology to distinguish species of pleurocerids.  So what might the mtDNA sequence data tell us about the genetic relationships between Whelan & Strong’s Pleurocera populations (all six of them) and Pleurocera populations sampled from elsewhere in the drainage of the Tennessee?  Tune in next time…


Notes:

[1] Dillon, R. T., S. J. Jacquemin & M. Pyron (2013)  Cryptic phenotypic plasticity in populations of the freshwater prosobranch snail, Pleurocera canaliculata.  Hydrobiologia 709: 117-127.  [PDF]

[2] Here are the complete locality data for all four sites mentioned in this month’s blog:
  • Site #1 – Tennessee River at Decatur, Morgan County, AL.  (34.6279N; -86.9564W).  This was site “CT” of Dillon et al. (2013).
  • Site #2 – Limestone Creek at Nick Davis Road, 2 km N of Capshaw, Limestone County, AL. 
  • (34.8027N; -86.8163W).  This was site “PT” of Dillon et al. (2013).
  • Site #4 - Paint Rock River at US 431 bridge, 25 km SE of Huntsville, AL.  (34.4992, -86.3905).
  • Site A – Estill Fork at Co. 140 bridge, Jackson Co, AL.  (34.9653, -86.1537).
[3]  Cryptic phenotypic plasticity in P. canaliculata:
  • Pleurocera acuta is Pleurocera canaliculata [3June13]
  • Pleurocera canaliculata and the process of scientific discovery [18June13]
[4] Dillon, R. T. (2011)  Robust shell phenotype is a local response to stream size in the genus Pleurocera (Rafinesque 1818). Malacologia 53: 265-277. [PDF]

[5] Cryptic phenotypic plasticity in P. clavaeformis:
  • Goodrichian Taxon Shift [20Feb07]
  • Mobile Basin III: Pleurocera Puzzles [12Oct09]
  • Goodbye Goniobasis, Farewell Elimia [23Mar11]
[6] Goodrich, C. (1940) The Pleuroceridae of the Ohio River system. Occas. Pprs. Mus. Zool. Univ. Mich., 417, 1-21.

[7] Whelan, N.V. & E. E. Strong (2016)  Morphology, molecules and taxonomy: extreme incongruence in pleurocerids (Gastropoda, Cerithiodea, Pleuroceridae). Zoologica Scripta 45: 62 – 87.  Open Access: [html]

[8]  I have featured the Leptoxis mtDNA data set of Whelan & Strong in three previous essays:
  • Mitochondrial Superheterogeneity: What we know [15Mar16]
  • Mitochondrial Superheterogeneity: What it means [6Apr16]
  • Mitochondrial Superheterogeneity and speciation [3May16]
[9] Our good friends Nathan Whelan and Ellen Strong seemed unaware that Conrad’s pyrenellum is an ecophenotypic variant of Say’s canaliculata, and indeed entirely neglected to cite the (2013) paper by Jacquemin, Pyron, and myself.  I’m sure this was just a simple oversight.

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