Editor’s Note – This essay was subsequently published as:
Dillon, R.T., Jr. (2019c) Mitochondrial superheterogenity: What it means. Pp 155 - 161 in The Freshwater Gastropods of North America Volume 3, Essays on the
Prosobranchs. FWGNA Press, Charleston.
Last month [1] we reviewed, or at least touched upon, 15
separate reports of double-digit mtDNA heterogeneity within gastropod
populations published over the last 20 years, the paper by Whelan & Strong [2]
among the best and most recent. Three
additional reports from pulmonate snail populations have subsequently come to
my attention [3]. The discussion
sections of almost all of these works have featured lists of possible
explanations for the phenomenon, including population fragmentation, great
antiquity, introgression from other species and cryptic speciation, many of
which do not seem to fit the data as it has now accumulated, none of which is
complete.
So Rob Dillon’s model to explain mitochondrial superheterogeneity
begins with an observation (not an assumption, in the case of pleurocerid snails)
of large numbers of super-isolated populations.
Then I add two more super-assumptions: super-long time and super-rare
dispersal events. And let me begin with
an extended analogy.
The even-toed ungulates first evolved in the Eocene Epoch,
about 50 mybp. So today, the mtCOI
sequence divergence between American bison (JF443195) and the wildebeest of the
Serengeti (JX436977) is approximately 15%.
I suggest that when we stand on the bank of the Green River in Polk
County, NC, and look down at the population of Pleurocera proxima grazing over
the rocks, it is as though we were Lewis and Clark, looking over a vast herd of
American bison [4]. And should we drive
80 km west to Buncombe Co, NC, and look down on the Pleurocera proxima
population inhabiting Bent Creek, it is as though we were Frederick Russell
Burnham standing before the wildebeests.
Now suppose that every million generations or so, a wading
bird with sticky feet transports one snail from Buncombe County to Polk County,
as though a modern zookeeper were to airlift a wildebeest to Wyoming. I don’t know, but it seems likely to me that
our jet lagged wildebeest might find itself perfectly well-adapted to graze on
the plains of Wyoming in all respects, morphologically and
physiologically.
But it does not seem likely to me that a single wildebeest
could reproduce in a herd of American bison.
I imagine a variety of prezygotic reproductive isolating mechanisms have
evolved between wildebeest and bison – appearances, smells, behaviors and so
forth. And even if a mating should
occur, I feel certain all sorts of postzygotic incompatibilities have evolved -
the chromosomes of the two species probably don’t match, a million screw ups
occur in development, and nothing comes of it.
So (I admit) the most implausible element of my model is
that, in the case of pleurocerid snails, a super-rare immigrant arriving via
sticky-bird express must successfully mate within a host population from which
it has been isolated for millions of generations. There are several factors that make this phenomenon
marginally less-implausible for pleurocerids, specifically. Pleurocerid snails are aphallic, and no
obvious mating behavior has been reported.
Apparently the male simply crawls over the female and deposits a
spermatophore in her gonoduct, so unceremoniously that human observers
typically don’t even notice it. There’s
very little light down where the snails live, so appearances don’t matter. And pleurocerid populations typically inhabit
waters with significant flow rates, so it seems unlikely that chemical mating cues
could evolve.
Now why postzygotic reproductive incompatibilities have not
evolved over millions of generations among such isolated gastropod populations,
I do not know. North American
pleurocerids seem to demonstrate negligible anatomical diversity [5], and
negligible chromosomal diversity to match [6].
I was tempted to add “super-stable environment” to my list of
assumptions in paragraph two at the top of this essay, because it seems
possible to me that stabilizing selection may have worked to prevent
reproductive isolating mechanisms from evolving.
But I should hasten to add that very little of the
reproductive biology I have reviewed directly above applies to pulmonate land
snails, and that it was in land snail populations mitochondrial superheterogeneity
was first discovered [7]. The bottom
line seems to be that, over a wide range of mating systems, populations as
isolated as bison and wildebeest have not speciated in gastropod world. The plains of snail-America and snail-Africa
are both grazed by reproductively compatible “wildebison.”
Rob Dillon’s patented “wildebison model” fits all six of the
points I reviewed last month regarding mitochondrial superheterogeneity as a
general phenomenon [1]. So let us return
to the Leptoxis population inhabiting Shades Creek in northern Alabama, marked
in dark blue above. Whelan & Strong
reported 16 copies of the modal CO1 sequence (the “bison” sequence, at red-star-15)
and one copy of a 12% divergent sequence, which we’ll call “wildebeest.” The wildebeest sequence almost exactly
matched the modal sequence in the Cahaba River at the US52 bridge, shown in
black above (at red-star-14). And not
only did the rare CO1 sequence of Shades Creek match the modal CO1 sequence of
the Cahaba River, the rare 16S sequence of Shades Creek matched the modal 16S
sequence of the Cahaba River. The
conclusion seems almost inescapable that at some point in the (probably
distant) past, a Cahaba wildebeest has been airlifted into the Shades Creek
bison population.
The first-most amazing thing about this data set is that an
individual Cahaba wildebeest was apparently able to mate into the Shades Creek
bison herd, despite millions of generations of isolation. And the second-most amazing thing is that
Whelan & Strong happened to sample both Shades Creek and the Cahaba River,
to show us what happened. In most data
sets of this sort, we simply find no clue.
So for example, in addition to the 17 copies of the modal
CO1 sequence Whelan & Strong reported from the Cahaba River at US52, they
also reported two copies of a 20% divergent sequence that matches nothing else
in their database, way off at red-star-11 [8, 9]. Did that rare mitochondrial genome come from
a third population of “wildecamels,” currently grazing on some other continent that
W&S did not sample? Or might that
genome have originated in an extinct population of “wilde-Irish-elk,” now
gone? A fascinating question.
I will close with two final notes. First, I should emphasize that I have not
evoked selection at any point during the essay above. I very nearly used the S-word when I was waving
my hands about the apparent absence of reproductive isolation among highly
isolated gastropod populations with a surprising range of evolutionary
backgrounds, but (ultimately) held off.
The wildebison model is grudgingly neutral.
And second, my good friend John Robinson and I are currently
simulating the evolution of mitochondrial superheterogeneity using the “ms”
program of R. R. Hudson [10]. Our
preliminary results have not yielded the phenomenon in single-population models
given any reasonable values of mutation rate (u) and population size (Ne). Our two-population models do, however, yield
mitochondrial superheterogeneity within reasonable values of u and (perhaps-surprisingly
low values of) Ne, given (super-rare) migration rates around Nem = 0.0001 genomes
per generation.
I find all this quite interesting as a study of evolutionary
science, pure as the driven snow, and (I feel sure) a large fraction of my
readership does as well. But in situations
such as the pleurocerid fauna of Alabama, research efforts have been at least
partly motivated by conservation concerns regarding the distribution of potentially
endangered species. What might mtDNA
sequence data sets such as developed by Whelan & Strong, riddled (as they
are) with superheterogeneity, tell us about the species relationships of the
populations sampled? Tune in next time!
Notes
[2] 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]
[3] Pinceel, J, K. Jordaens & T. Backeljau
(2005) Extreme mtDNA divergences in
a terrestrial slug (Gastropoda, Pulmonata, Arionidae): Accelerated evolution,
allopatric divergence and secondary contact.
J. Evol. Biol. 18: 1264 – 1280. Parmakelis, A., P. Kotsakoizi & D. Rand
(2013) Animal mitochondria, positive
selection and cyto-nuclear coevolution: Insights from Pulmonates. PLOS ONE 8(4): e61970. Nolan, J. R., U. Bergthorsson
& C. M. Adema (2014) Physella
acuta: atypical mitochondrial gene order among panpulmonates (Gastropoda). J. Moll. Stud. 80: 388 – 399.
[4] The populations of Pleurocera I’m using as examples here
were sampled in 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]. I reviewed the Dillon & Robinson results in my blog post
of March, 2009. See:
- The Snails The Dinosaurs Saw [16Mar09]
[6] Dillon, R.T. (1989)
Karyotypic evolution in pleurocerid snails. I. Genomic DNA estimated by flow
cytometry. Malacologia 31: 197-203. [PDF]
Dillon, R.T. (1991) Karyotypic
evolution in pleurocerid snails. II. Pleurocera, Goniobasis, and Juga.
Malacologia 33: 339-344. [PDF]
[7] I almost cut the
two paragraphs about the absence reproductive isolating mechanisms in
pleurocerid snails entirely out of this essay.
But then I figured, hell, if the land snail people don’t like it, they
can start their own blog.
[8] For this
calculation I used KT164003 as an example as the modal CO1 sequence from the
Cahaba River at US52, and KT164004 as an example of the rare, divergent
sequence, and compared the two using blastn.
[9] And somewhat amazingly, Whelan & Strong also found one
mitochondrial haplotype in the Cahaba River at US52 that matches the Shades
Creek mode. So their Figure 4
(reproduced above) should have shown one little black circle near their big
blue circle, as well as that single little blue circle near their big black. I have added one little black circle at red-star-15
above. More about this next month.
[10] Hudson, R. R. (2002)
Generating samples under a Wright-Fisher neutral model of genetic
variation. Bioinformatics 18:
337-338.