Editor’s Note – This is the third installment of a three-part series reviewing the 2022 paper by Whelan and colleagues [1] on “Prodigious polyphyly in the Pleuroceridae.” We recommend that you back up and read both our posts of September [23Sept25] and October [14Oct25] if that material isn’t fresh in your mind. You will also find our posts of [6Apr23] and [9May23] helpful as background for the essay that follows, if you want to dig more deeply into the subject matter itself.
Back in early September I enjoyed a wonderful two-week field trip to the Ozark/Ouachita Highlands of Arkansas, southern Missouri, and eastern Oklahoma, logging 3,700 miles on my pickup and 20 miles on my kayak, collecting 59 sites. And I am looking forward to sharing a lot of stories about my adventures in that biogeographically fascinating part of the world with you all in future posts. Some of the observations I made on Leptoxis arkansensis during that memorable excursion are, however, especially relevant to the “prodigious polyphyly” discovered by Nathan Whelan and his colleagues [1] in the AHE phylogenomic study we are currently reviewing.
Populations of Leptoxis arkansensis are uncommon and widely scattered in the region, primarily inhabiting the rocky riffles of small rivers with good water quality, always (as far as I can tell) co-occurring with large and nearly-omnipresent populations of Pleurocera potosiensis. From all evidence, the two are distinct biological species. The shells born by L. arkansensis demonstrate a larger body whorl than those of P. potosiensis, consistently and reliably, from birth to maturity. But their grossly similar morphology in overall shell form can render the two species difficult to distinguish in the field. There is not a shadow of doubt in my mind that they are “sister” species, one evolved from the other.
The strongest hypothesis, I would suggest, is that the original population of Leptoxis arkansensis evolved from a Pleurocera potosiensis population specialized for life in the riffles at midstream, and that the larger body whorl reflects a relatively larger foot, adapted for clinging to rocks in rapid currents. Might that same adaptation have evolved more than once in the hundred-million-year history of the North American Pleuroceridae? Who among my vast and erudite readership could imagine any answer to my rhetorical question other than the affirmative [2]?
My loyal readership might remember a (rather personal) essay I posted back in [6Apr23], “Growing Up With Periwinkles.” In that post I reviewed my own 60+ years of experience with Leptoxis in the Southern Appalachians, from childhood through college and into my professional career, including several allozyme studies and even one (rather atypical, for me) sequence study as well. I concluded that essay as follows: “If you had asked me ten years ago, I would have listed six valid species of Leptoxis in North America: carinata, praerosa, crassa, picta, plicata, and maybe that weirdo way out in the Ozarks, Leptoxis arkansensis (Hinkley 1915), I have no reason to doubt.”
Then, in the essay that followed [9May23], I “tested the periwinkle hypothesis” with the four-gene phylogeny (CO1, 16S, 28S, H3) that Nathan Whelan developed for his (2013) dissertation [3], finding solid agreement with my six-species model. The main trunk of Nathan’s gene tree showed L. praerosa, L. crassa, L. carinata and L. picta distinct as expected. Leptoxis plicata and L. arkansensis were also distinct, but depicted way off in the distant foliage with a variety of pleurocerids representing other genera.
There was also one surprise – evidence of a cryptic species sympatric with Leptoxis praerosa through much of their shared range in East Tennessee and North Alabama. Nathan identified that cryptic species, quite problematically, as Leptoxis virgata. At the end of my [9May23] essay I had renamed my hypothesis for the genus Leptoxis in North America the 6* Species Model, adding that asterisk for the possibility of a seventh, cryptic species.
 |
| Figure 4 of Whelan et al [1] |
Both of those 2023 essays were focused entirely on evolutionary relationships at the species level and below. I wouldn’t say that I myself am entirely disinterested in evolution at higher levels, it just seems to me that we ought to work out some plausible hypotheses for the populations and the species first. So now, with the 6* Species Model firmly supported both by Nathan’s 4-gene dissertation and by my own 60+ years of experience in field and laboratory, we are in a position to understand what Nathan’s more recent AHE phylogenomic analysis is telling us about the evolution of Leptoxis as a genus. Then starting at three o’clock, and proceeding clockwise:
Leptoxis picta. Way back in 1998, our good buddy Chuck Lydeard and I published a paper [4] showing that the allozyme divergence among six populations of three nominal species of Alabama Leptoxis: L. picta, L. ampla, and L. taeniata (subsequently [5] renamed coosaensis), was no greater than the divergence among control Leptoxis populations sampled from the Tennessee drainage, which nobody had ever suggested were anything other than L. praerosa. We suggested that those three Mobile Basin nomina be united under the oldest name, Leptoxis picta (Conrad 1834).
Since 1998, an impressive body of research has been published supporting that hypothesis. Nathan’s four-gene dissertation [3] returned negligible divergence among picta, ampla, taeniata/coosaensis, and foremani (7 populations, 18 individuals). And both of Nathan’s (really quite lovely) subsequent studies of interpopulation divergence in “Leptoxis ampla,” his (2016) study of mitochondrial superheterogeneity [6] and his (2019) RADseq study [7], recovered strikingly high levels of interpopulation divergence, which easily extrapolate to include Mobile Basin populations historically identified as picta, taeniata/coosaensis, and foremani.
Now open before us we have a fifth study, estimating levels of genetic divergence among 192 individual pleurocerid snails over their entire single-copy genomes using the cutting-edge technique of Anchored Hybrid Enrichment, showing exactly the same result as references [3], [4], [6], and [7]. The nomina ampla, coosaensis, foremani and taeniata are all obsolete, junior synonyms of L. picta. And to find the branches of a 21st century phylogenomic tree cavalierly decorated all about its entire periphery with 19th century superstition is an embarrassment to our entire profession.
Leptoxis carinata. Quite independently of the evolution of Leptoxis picta in the Mobile Basin of Alabama, Nathan’s AHE phylogenomic analysis suggests a second origin of the genus Leptoxis in the southern Appalachians. This origin is likely much older.
The sequencing studies I published with John Robinson in 2009 confirmed that Ohio drainage populations identified as Leptoxis dilatata (Conrad 1835) are conspecific with Atlantic drainage populations identified (since 1792!) as Leptoxis carinata, and suggested that the pleurocerid fauna of this ancient region might have evolved at the (Paleozoic) Appalachian orogeny [8]. Both the conspecific status of the two nomina, and the origin of Leptoxis carinata (now more broadly and properly understood) independent of any other Leptoxis species, were confirmed by Nathan’s dissertation [3], and have now been triple-checked by the AHE phylogenomic analysis under review here.
Leptoxis crassa and praerosa. Again dovetailing nicely with his (2013) dissertation research, Nathan’s big AHE phylogenomic analysis confirms that Leptoxis crassa (identified here under the obsolete [9] synonym “Athearnia anthonyi”) is related to, but specifically distinct from, Leptoxis praerosa. And the larger set of crassa + praerosa together apparently represents a third independent evolution of the shell morphology we associate today with the genus Leptoxis. This third origin seems to have occurred in the Tennessee/Cumberland region, I should guess after Leptoxis carinata evolved further east, but before L. picta to the south.
Burrowing more deeply into that lovely lavender subcluster, we find further confirmation of Nathan’s 2013 results suggesting that umbilicata (Weatherby 1876) and subglobosa (Say 1825) are junior synonyms of L. praerosa (Say 1821). Somewhat surprisingly, however, Nathan’s AHE analysis did not return evidence of any significant genetic distinction between two individuals he identified as L. virgata (only one of which is depicted below) and the larger L. praerosa cluster.
You might recall from my [9May23] review of Nathan’s dissertation that he did not specify any morphological trait by which his L. virgata could be distinguished from sympatric populations of L. praerosa, and that the genetic difference was apparently only mitochondrial, not nuclear. Here ten years later, we are left wondering whether Nathan might have misidentified both of his nominal virgata specimens in 2022, or if the evidence he adduced in 2013 that a second biological species might be cryptic under our old friend Leptoxis praerosa might have been an atypically widespread case of mitochondrial superheterogeneity [11].
Leptoxis
arkansensis. We reviewed this branch of Nathan's AHE phylogenomic tree at the top of this essay. The independent origin of Leptoxis
arkansensis way out west in the Ozark highlands seems to be yet a fourth
evolution of the shell morphology we associate today with the genus
Leptoxis.
Leptoxis
plicata. Even as the 1998 allozyme study
of Dillon & Lydeard [4] was returning conspecific levels of genetic
divergence among Alabama populations of Leptoxis picta, ampla, and
taeniata/coosaensis, a fourth nominal species of Leptoxis from the state of
Alabama, Leptoxis plicata, was revealed to be genetically distinct. The single population of L. plicata known at
that time, inhabiting the Locust Fork of the Black Warrior River, bore shells
with a characteristically high apex and weak but distinctive plication on the
upper whorls.
 |
| From Whelan et al [1] |
Regarding that parenthetical modifier, “almost.” I did not mention it at the time of my [9May23] review, but it is certainly worthy of note today, that in 2013 Nathan seems to have found very little sequence divergence between Leptoxis plicata and a newly-rediscovered Leptoxis population inhabiting the Cahaba River about 50 km south of Locust Fork, which he identified as Leptoxis compacta [13]. Here’s the copy of Nathan’s gigantic Baysian tree that I first made available for download from my 2023 review, with the little plicata/compacta cluster encircled in red:
Now here ten years later, we find Leptoxis plicata and L. compacta again depicted as conspecific in Nathan’s AHE phylogenomic tree. I myself have no biological insight to contribute, my experience with the legendary pleurocerid fauna of the Cahaba River being limited to song, story, and musty chronicle. The descriptions I have read and the figures I have seen of the L. compacta shell do not mention shell plication, but do show the same unusually high spire characteristic of L. plicata.
In any case, I am sure we can all agree that the shell morphology borne by the Locust Fork / Cahaba pleurocerid populations together, clustered as they are upon the far-flung branches of every gene tree they’ve ever hung, suggests yet another separate origin of the genus Leptoxis.
So, to
summarize the first 71% of the present essay.
Nathan’s AHE phylogenomic analysis confirms the 6-Species Model for the
genus Leptoxis, without an asterisk. The
rocky shoals of North American rivers are inhabited by, in order of their
description, Leptoxis carinata (Brug. 1792), L. praerosa (Say 1821), L. picta
(Conrad 1834), L. plicata (Conrad 1834), L. crassa (Hald. 1841), and L.
arkansensis (Hinkley 1915). And the
shell morphology that has historically served to unite these six biological
species into the genus Leptoxis has evolved five separate times.
The
first genus-level name to be proposed for the freshwater cerithiaceans of North
America was, apparently [14], Pleurocera. And it was the eccentric French
naturalist Constantine Rafinesque who did the proposing, way back in 1818. The shell that he seems to have had in his
hand at that time was elongate, with a high spire and small body whorl,
best-guess-identified today as Pleurocera canaliculata [15].
And the
second genus-level name proposed for the North American freshwater
cerithiaceans was like unto the first, also proposed by Rafinesque, one year
later. That genus name was Leptoxis. And the shell that Rafinesque seems to have
had in his hand at that juncture was rotund and obovate, with a low spire and a
large body whorl, best-guess-identified today as Leptoxis praerosa [15].
Thus, it
seems that even prior to the birth of American malacology, when Frenchmen were
still running around loose in our backwoods with butterfly nets, everybody who
has ever pulled more than one pleurocerid snail out of our crystal-clear waters
has divided out a subset bearing shells that are elongate and a subset bearing
shells that are obovate.
 |
| Rafinesque (1783-1840) |
No. The binomial system of nomenclature was not
first proposed by Carl Linnaeus in 1758 for any evolutionary purpose
whatsoever. It was first a tool for
information storage and retrieval, and it served that function alone for its
first 100 years of application, carrying Darwin toward the Theory of Evolution
just as surely as The Beagle. And that
information-retrieval function continues to be the primary utility of
biological taxonomy even to the present day.
I
absolutely understand that the names of organisms must be changed to reflect
scientific advance, and have certainly done my fair share of the changing. But when we change a name, we pay the price of
losing some of the information the previous name historically transmitted.
The only
reason I synonymized Goniobasis and Elimia under Pleurocera in 2011 [16] was my
discovery that single randomly-breeding populations of freshwater gastropods
were being classified into three genera – not just in one case, but repeatedly,
throughout the North American pleurocerid fauna. The cost of the misinformation being generated by the
Pleurocera/Goniobasis/Elimia confusion outweighed, in my judgement, the cost of the information lost by the combination of those three names.
And I
would invite Nathan Whelan and all our mutual colleagues, once again, to follow suit
on that. Look at that tangle of blue and
yellow branches in the GHIJKL quadrant of your tree, colleagues! Your own analysis shows that there is no
evolutionary basis for the genus name “Elimia.”
I
understand your fervent desire to preserve obsolete nomina for the information they
transmit. I would point out, however,
that “Goniobasis” contained even more information than “Elimia” when Burch [10]
high-handedly dumped Goniobasis for an obscure point of taxonomic priority in
1980, yet our discipline survived. And I
would argue that the profits we all stand to gain by correcting the
misinformation being promulgated even unto the present day by the entirely
artificial distinction [17, 18] between Elimia and Pleurocera far outweigh the information
losses we will suffer synonymizing the former under the latter.
But as
to the other Burch/Goodrich genera – Lithasia, Io, Gyrotoma and especially
Leptoxis, I believe that we have now reached consensus. Can we all agree to take Queen Elsa’s advice,
henceforth? Let it go.
Notes:
[1]
Whelan, N. V., Johnson, P. D., Garner, J. T., Garrison, N. L., & Strong, E.
E. (2022). Prodigious polyphyly in Pleuroceridae (Gastropoda: Cerithioidea).
Bulletin of the Society of Systematic Biologists, 1(2).
https://doi.org/10.18061/bssb.v1i2.8419
[2] Here
I have answered a rhetorical question with a second rhetorical question. And this isn’t even rhetoric, it is
prose. Have I violated some ancient and
hoary guideline? If so, I plead ignorance,
and apologize.
[3]
Whelan, Nathan V. (2013) Conservation, life history and systematics of Leptoxis
Rafinesque 1819 (Gastropoda: Cerithioidea: Pleuroceridae). PhD Dissertation, University of Alabama,
Tuscaloosa. 179 pp. For a review, see:
- Testing the periwinkle hypothesis [9May23]
[4] Dillon, R.T., and C. Lydeard (1998) Divergence among Mobile Basin populations of the pleurocerid snail genus, Leptoxis, estimated by allozyme electrophoresis. Malacologia. 39: 111-119. [pdf]
[5]
Whelan, Nathan V.; Johnson, Paul D.; Garner, Jeffrey T.; Strong, Ellen E.
(2017). On the identity of Leptoxis taeniata – a misapplied name for the
threatened Painted Rocksnail (Cerithioidea, Pleuroceridae). ZooKeys (697):
21–36. https://zookeys.pensoft.net/article/14060/
[6]
Whelan, N.V. & E. E. Strong (2016) Morphology, molecules and taxonomy:
extreme incongruence in pleurocerids (Gastropoda, Cerithiodea, Pleuroceridae).
Zoologica Scripta 45: 62 – 87. For a
review, see:
- Mitochondrial superheterogeneity and speciation [3May16]
[7] Whelan, N.V., M.P. Galaska, B.N. Sipley, J.M. Weber, P.D. Johnson, K.M. Halanych, and B.S. Helms (2019) Riverscape genetic variation, migration patterns, and morphological variation of the threatened Round Rocksnail, Leptoxis ampla. Molecular Ecology 28: 1593 – 1610. For a review, see:
- Intrapopulation gene flow, the Leptoxis of the Cahaba, and the striking of matches [2Nov21]
[8] 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. [pdf] For a review, see:
- The snails the dinosaurs saw [16Mar09]
[9] Jack
Burch [10] lowered “Athearnia” to subgeneric status under Leptoxis way back in
1980, as he lowered “anthonyi” to subspecific status under crassa. The relentlessly archaic taxonomy to which
Nathan Whelan and his colleagues cling is not even current to the 20th century,
much less the 21st.
[10]
This is a difficult work to cite. J. B.
Burch's North American Freshwater Snails was published in three different
ways. It was initially commissioned as
an identification manual by the US EPA and published by the agency in
1982. It was also serially published in
the journal Walkerana (1980, 1982, 1988) and finally as stand-alone volume in
1989 (Malacological Publications, Hamburg, MI).
[11] The
phenomenon of mitochondrial superheterogeneity was first documented in the
pleurocerid snails by Dillon & Frankis [12] and made famous in 2009 by
Dillon & Robinson [8]. The term was
not actually coined until 2016, however, in a series of posts on this
blog. See:
- Mitochondrial superheterogeneity: What we know [15Mar16]
- Mitochondrial superheterogeneity: What it means [6Apr16]
- Mitochondrial superheterogeneity and speciation [3May16]
[12]
Dillon, R. T., and R. C. Frankis. (2004) High levels of DNA sequence divergence
in isolated populations of the freshwater snail, Goniobasis. American Malacological Bulletin 19: 69 - 77 [pdf].
[13]
Whelan NV, Johnson PD, Harris PM (2012) Rediscovery of Leptoxis compacta
(Anthony, 1854) (Gastropoda: Cerithioidea: Pleuroceridae). PLoS ONE 7(8):
e42499. https://doi.org/10.1371/journal.pone.0042499
[14] The
actual meaning of Rafinesque’s 1818 nomen “Pleurocera” was shrouded in mystery
and roiled by controversy for many years. For a
review, see:
- Joe Morrison and the great Pleurocera controversy [10Nov10]
[15]
Both Pleurocera canaliculata and Leptoxis praerosa were described by Thomas Say
in 1821. Yes, it is possible to describe
a genus before its type species.
[16]
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]. For a
review, see:
- Goodbye Goniobasis, Farewell Elimia [23Mar11]
[17] For
a demonstration of the artificiality of the genus nomen Elimia, see:
- Goniobasis and Elimia [28Sept04]
[18] And
for a demonstration of the artificiality of the genus nomen Goniobasis, see:
- A House
Divided [10May20]
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