Reticulate Evolution in the North American Pleuroceridae

Last month [15Oct24] we reviewed the evidence that populations of two pleurocerids widespread in the Greater Ohio Drainage, P. laqueata and P. troostiana, hybridize extensively in the rivers and streams of Middle Tennessee.  And our most useful genetic marker was shell plication, a scallop-shaped ridging pattern characteristic of P. laqueata, absent from P. troostiana outside the laqueata range, but variably present in troostiana populations overlapping with laqueata.

Sharing most of those same rivers and streams with both laqueata and troostiana are populations of a third pleurocerid species, P. simplex, our old friend familiar from five previous essays, see footnote [1] below to refresh your memory.  The FWGNA Project recognizes two subspecies of simplex: the typical form found in small streams throughout the greater Tennessee/Cumberland region and a paler, more heavily shelled form common in larger streams of the Cumberland drainage, extending into Central Kentucky, Pleurocera simplex ebenum.

In 1934, Calvin Goodrich [2] published #3 in his “Studies on the gastropod family Pleuroceridae” series, focusing on shell plication.  Here is a verbatim quote from page 5:

“G. ebenum (Lea), commonly a smooth species, occurs in the Cumberland River drainage basin. In the upper part of the drainage, material containing plicate shells has been taken. The only lot at hand that can be accepted as a “pure" race of these forms is from New River, Scott County, Tennessee. Of 46 shells from Straight Creek at Pineville, Bell County, Kentucky, 54.4 per cent are plicate. In the Cumberland River a few miles below Pineville, 18 per cent of 72 shells are so sculptured; 74 shells of ebenum taken just above the falls of the Cumberland are 14.8 per cent plicate. The only specimens from the river below the falls which have been seen, taken at Smith's Shoals near Burnside, Pulaski County, Kentucky, are all smooth; so also are shells of all lots of the species ranging as far to the west as streams of Dickson County, Tennessee.”

Yes, all of that is true.  I myself have confirmed at least seven populations of P. simplex ebenum bearing lightly plicate shells scattered about Middle Tennessee, in minor tributaries of the Cumberland, the Harpeth, the Red, and the Duck.  All these populations co-occur with populations of P. simplex bearing normal, smooth shells and populations of (you guessed it) P. laqueata.  The first three shells figured at left below were collected from the backs of pleurocerids inhabiting Brush Creek, a tributary of the Red-Cumberland in Robertson County, NW of Nashville (36.4342, -87.0662): an apparently pure P. simplex, an apparently pure P. laqueata, and what most certainly appears to be a simplex/laqueata hybrid (“castanea”), almost entirely smooth but bearing tiny plications around the apex.

Reticulate evolution in the Pleuroceridae

Exactly as is the case with P. troostiana, P simplex populations inhabiting East Tennessee, where P. laqueata does not occur, never bear plicate shells.  Only where the ranges of P. simplex and P. laqueata overlap in Middle Tennessee does one find pleurocerid populations bearing fat, pear-shaped simplex-looking shells with tiny apical plications.

There is not a shadow of doubt in my mind that P. simplex hybridizes with P. laqueata, just as P. laqueata hybridizes with P. troostiana.  The two shells at right were sampled from Spring Creek east of Nashville, carried over from last month: an apparently pure P. troostiana and a laqueata/troostiana hybrid (“perstriata.”)  This is reticulate evolution.

Digging back through the classic literature, it turns out that Isaac Lea described a Melania castanea in 1841, the shell of which appears to be a perfect match for the simplex/laqueata hybrid populations I have been referring to here.  Lea’s brief Latinate description appeared in that same early work that featured such notables as clavaeformis, ebenum, and edgariana [3], with a longer English description and figure following in 1843 [4].  Lea’s type locality, “Maury County, Tenn.” is in the upper Duck River drainage, where simplex and laqueata are both common.  Calvin Goodrich [5] lowered Lea’s nomen castanea to subspecific status under Goniobasis laqueata in 1940, giving its range as “Headwaters of the Duck River, Tennessee.”

Melania castanea [4]

OK, fine.  Given that we have recognized three subspecific names for laqueata/troostiana hybrids, I suppose it is only fair to recognize a subspecific name for hybrids between P. laqueata and P. simplex.  So, this week I have added a new (sub)species page to the FWGNA website for Pleurocera laqueata castanea (Lea 1841), with corresponding entries in the gallery and dichotomous key for the Tennessee/Cumberland [6].  This is the 135th species or subspecies of freshwater gastropod we have recognized as valid in our 21-state study region.

I am every bit as certain that P. simplex hybridizes with P. semicarinata in Kentucky and Tennessee, although I have no genetic data or photos to enter into evidence.  The two species are only distinguishable by subtle differences in shell shape, the former bearing fatter shells with a larger body whorl, neither demonstrating any sort of shell sculpture (beyond a carinate upper whorl) that might serve as a discrete marker.  The range of P. semicarinata semicarinata overlaps that of P. simplex broadly in the Cumberland, Green, and Kentucky Rivers, and extends much further north, up into Wisconsin, Michigan and New York, where chubby-shelled populations are referred to the subspecies P. semicarinata livescens.

And I am still amazed [7] by the 1994 allozyme study of Bianchi and colleagues [8] demonstrating hybridization between Great Lakes P. semicarinata livescens and the Hudson River population of Pleurocera virginica through the Erie Canal.  Those two species bear strikingly different shell morphologies, have entirely distinct ranges, and could not have shared a common ancestor in many, many millions of years.  Perhaps since the Appalachian Orogeny?

Hybridizing? [9]

Yes, that is my next point.  The architects of the Modern Synthesis generally seem to have considered hybrid zones an unstable and transitory step toward speciation [11].  I am sympathetic with the Darwinian rationale for such an hypothesis, and admit it could certainly hold in many cases.  But more recently the research emphasis seems to have shifted toward hybrid zones that give evidence of stability and permanence [12].

The photo below comes from the 8Mar24 issue of Science [13].  Here’s the caption: “This fish is the hybrid offspring of an alligator gar and a spotted gar – members of genera that last shared a common ancestor at least 100 million years ago.”

The paper reviewed, by Brownstein and colleagues [14], detailed the results of a survey of 1,105 exons over 481 vertebrate species, demonstrating exceptionally slow rates of molecular evolution in gars and sturgeons.  Yet gar species last sharing a common ancestor no later than the Cretaceous still hybridize naturally in the greater Ohio and southern Mississippi drainages today.

Could some cranky, washed-up old crackpot wading those same rivers and streams, throwing snails into a bucket and measuring them with rusty calipers, achieve the same results as an international team of eight scientists from six different institutions with “massive” DNA data sets and ten different sources of funding?

The distribution of pleurocerid snails in the rivers and streams of North America is whispering a story to us in a language that we do not understand.  It is an ancient story of colliding continents and earthquakes and mountains 10,000 feet high, eroding and shifting and washing into the sea.  Most of the pleurocerids of the Greater Ohio drainage, including P. simplex and P. troostiana, range across the entirety of the state of Tennessee, as well as into Kentucky and North Alabama and even into SW Virginia.  Then why are populations of P. laqueata absent East of Chattanooga?  Is their dispersal capability so much poorer than P. simplex and P. troostiana that they are unable to penetrate Walden’s Ridge?  I simply do not think so.  Here is the story that I hear the pleurocerids whispering to me.

The story I hear is that the crest of the ancient Appalachians, at some point in the millions of years of their orogeny, was approximately where Walden’s Ridge lies today, at the eastern edge of the Cumberland Plateau.  Pleurocera laqueata evolved on the west side of that crest, while P. troostiana and P. simplex evolved on the East.  Then the mountains eroded such that the divide shifted east, opening a hole at Chattanooga, switching the flow of the rivers in which troostiana and simplex evolved from east to west, bringing those pleurocerid populations into secondary contact with laqueata.

I have said it many times [15], but I will say it again.  A step off the creek bank in the Southern Appalachians is a step back millions of years.  Look around you, colleagues, look!  Those banks are covered with mosses and liverworts, horsetails and ferns.  The waters team with dragonflies and stoneflies, gars and hellbenders.  And pleurocerid snails jostle each other to graze across every square inch of substrate.

Why does this entire ecosystem seem frozen in time?  My hypothesis calls on three independent sets of factors: environmental, genetic and historical.

First, the freshwater environment is more stable than that of the land.  Water temperatures lag behind and buffer air temperatures.  That buffer is not just seasonal, it is climatological.  The temperature in smaller streams, in particular, typically remains very close to that of the ground, 10 – 15 degrees Centigrade year round.  Such environments are not simply protected from hot Julys, they are protected from ice ages.  And the lower the temperature of the environment, I might add, the slower the generation times of its poikilothermic biota.

Rock Island State Park, TN [16]

Rainfall and storm are similarly buffered.  Droughts obviously have less effect on rivers than on the surrounding land, ditto wind and fire.  The ecosystems of many (especially smaller) bodies of water are based on allochthonous input, rather than primary productivity, and life could more easily survive (let us say) a cometary impact, and a period of worldwide darkness.

Most of the above, it must be admitted, could also be said for the marine environment as well as the freshwater.  This calls upon a second set of factors, which are population genetic.

In two words, marine populations are gigantic and panmictic.  Almost all the mollusks, for example, retain a planktonic larval stage lasting at least a couple weeks, facilitating dispersal over very long distances.  Here on the Atlantic side, the population of commercially important eastern quahogs (“cherrystone” or “littleneck” clams), demonstrates no significant allelic frequency differences at multiple allozyme-encoding loci from Canada to Florida [17].  Ditto oysters, ditto oyster drills, ditto whelks, ditto periwinkles [18].

Consequently, when a beneficial mutation arises in a marine population, it spreads quickly in evolutionary time.  Diseases, predators, and other riders of the apocalypse spread as quickly as the angels.  Speciation is quick, extinction is quick, evolution is quick.  The marine molluscan fauna of the Virginia Pliocene does not look like the marine molluscan fauna of the Virginia Recent.

But for better or worse, freshwater populations are small and fragmented.  Evolution does not stop, of course; the molecular clock keeps ticking [19].  But when adaptations evolve (such as reproductive isolation, for example) they do not spread [20, 21].  The outward appearances of such populations, then, will give the impression of morphological stasis.

So, freshwaters are more environmentally stable than the land, and the populations inhabiting those freshwaters more genetically stable than those inhabiting the sea.  There is a third factor.  History.

The land mass that we today identify as the “Appalachians,” together with the freshwaters that drain those mountains to the ocean, is really, really old.  It is clear that several orogenies have taken place, beginning with the Grenville over one billion years ago, proceeding through the Taconic (500 mybp) and the Acadian (400 mybp), culminating with the Alleghanian Orogeny at the formation of Pangaea 300 mypb.

Did Cerithiacean gastropods crawl from the sea at that time, evolve into the first pleurocerids, disperse and diverge across drainage systems as they existed in the ancient Appalachians hundreds of millions of years ago, and then sit in evolutionary stasis as the mountains wore down around them?  Yes, I think so.

Next month… taxonomic implications.

Notes:

[1] See the following essays for a review of the biology of Pleurocera simplex, its sibling gabbiana and its subspecies ebenum:

• The cryptic Pleurocera of Maryville [13Sept16]
• The fat simplex of Maryville matches type [14Oct16]
• CPP Diary: Yankees at The Gap [4Aug19]
• CPP Diary: What is Pleurocera ebenum? [3Oct19]
• CPP Diary: The spurious Lithasia of Caney Fork [4Sept19]

[2] Goodrich, C. (1934)  Studies of the gastropod family Pleuroceridae – III.  Occasional Papers of the Museum of Zoology, University of Michigan 300: 1 – 11.

[3] Lea, Isaac (1841) Continuation of Mr. Lea's paper on New Fresh Water and Land Shells.  Proceedings of the American Philosophical Society 2: 11 – 15.

[4] Lea, Isaac (1843)  Description of New Fresh Water and Land Shells.  Transactions of the American Philosophical Society 8: 163 – 250.

[5] Goodrich, C. (1940) The Pleuroceridae of the Ohio River drainage system.  Occasional Papers of the Museum of Zoology, University of Michigan  417: 1-21.

[6] Alas, Pleurocera laqueata castanea cannot be retroactively included in the hardcopy FWGNA Volume 5, which came off the presses in the fall of 2023.  In our next edition, however, castanea will be FWGNA species Number 103.2.

[7] See my essay of 3Mar22 for rankings of a broad selection of freshwater gastropod papers by international amazingness units. The paper of Bianchi et al [8] scored a whopping 93.2 iau, good for first place in the population genetics subdivision:

• The third-most amazing research results ever published for the genetics of a freshwater gastropod population. And the fourth-most amazing, too. [3Mar22]

[8] Bianchi, T. S., G. M. Davis, and D. Strayer 1994.  An apparent hybrid zone between freshwater gastropod species Elimia livescens and E. virginica (Gastropoda: Pleuroceridae).  Am. Malac. Bull. 11: 73 – 78.

[9] From left to right.  Pleurocera simplex simplex from Brush Creek, Robertson Co, TN (see above).  Pleurocera simplex ebenum from the Falls of The Cumberland, Whitley Co, KY [see 3Oct19].  Pleurocera semicarinata semicarinata from Harrison Ck, Nelson Co, KY [see 6Sept17]. Pleurocera semicarinata livescens from Portage Ck, Washtenaw Co, MI [10]. Pleurocera virginica, an especially chubby shell from Deer Ck, Harford Co, MD courtesy R. Aguliar.

[10] “Station 2” of Dazo, B. C. (1965)  The morphology and natural history of Pleurocera acuta and Goniobasis livescens (Gastropoda: Cerithiacea: Pleuroceridae).  Malacologia 3: 1 – 80.

[11] Dobzhansky, T. (1940) Speciation as a stage in evolutionary divergence. American Naturalist 74: 312 – 321.

[12] Barton, N.H. and G.M. Hewitt (1985) Analysis of hybrid zones.  Annual Review of Ecology and Systematics 16: 113-148.

[13] Heidt, A. (2024) Gars truly are “living fossils,” massive DNA data set shows.  Science 383 (6687): 1041.

[14] Brownstein, Chase B, Daniel J MacGuigan, Daemin Kim, Oliver Orr, Liandong Yang, Solomon R David, Brian Kreiser, and Thomas J Near (2024) The genomic signatures of evolutionary stasis.  Evolution 78: 821 – 834. https://doi.org/10.1093/evolut/qpae028

[15] Dillon, R T. and J. D. Robinson (2009)  The snails the dinosaurs saw: Are the pleurocerid populations of the Older Appalachians a relict of the Paleozoic Era?  Journal of the North American Benthological Society 28: 1 - 11.  (Rosemary Mackay Award)  [pdf].  For a review, see:

• The snails the dinosaurs saw [16Mar09]

[16] The Caney/Collins River system, impounded below Rock Island State Park, was home to at least eight species of pleurocerid snails, including P. simplex [4Sept19], P. troostiana edgariana [5June20] and the pleurocerid megafauna hung in Cousin Bob Winter’s prehistoric necklace as depicted [5Apr22].

[17] The population genetic literature on Atlantic coastal bivalves is very large.  For a review of the Mercenaria case, see:

• Dillon, R.T. and J.J. Manzi (1992) Population genetics of the hard clam, Mercenaria mercenaria, at the northern limit of its range.  Canadian Journal of Fisheries and Aquatic Sciences 49:2574-2578. [pdf]

[18] For reviews of the genetics of marine gastropod populations on the Atlantic coast, see:

• Wise, J., M. G. Harasewych, and R. T. Dillon. (2004)  Population divergence in the sinistral Busycon whelks of North America, with special reference to the east Florida ecotone.  Marine Biology 145:1167-1179. [pdf]
• Dayan, N.S., and R.T. Dillon (1995) Florida as a biogeographic boundary: Evidence from the population genetics of Littorina irrorata. The Nautilus 108: 49-54. [pdf]

[19] An inexorable (but not especially clocklike) accumulation of neutral mutations yields the startlingly high levels of mtDNA sequence divergence often recorded among pleurocerid populations.  And the crazy distribution patterns of those crazy mtDNA sequence markers come from rare long-distance dispersal events which, given hundreds of millions of years of birds wading through these streams and flying off elsewhere, do happen.  For more about my Jetlagged Wildebeest Model of mitochondrial superheterogeneity, see:

• Mitochondrial superheterogeneity: What we know [15Mar16]
• Mitochondrial superheterogeneity: What it means [6Apr16]
• Mitochondrial superheterogeneity and speciation [3May16]

[20] The absence of any correlation between genetic divergence and environmental difference in isolated populations of Pleurocera proxima, together with strong correlations between genetic divergence and geographic distance, supports this hypothesis.  See:

• Dillon, R.T. (1984) Geographic distance, environmental difference, and divergence between isolated populations. Systematic Zoology 33:69-82. [pdf]

[21] Evidence from Pleurocera proxima transplant experiments is also consistent with the hypothesis that beneficial genomes may be prevented from spread by the isolated character of southern Appalachian streams.  See:

• Dillon, R.T. (1988) Evolution from transplants between genetically distinct populations of freshwater snails. Genetica 76: 111-119. [pdf]