Terminally confused by "living fossils"

I picked up The Structure of Evolutionary Theory today for a mostly unrelated reason, and happened across this passage:

(Ironically, stable lineages become salient enough to catch our attention only at the extreme that we call "living fossils" -- species or lineages supposedly unchanged during such long stretches of geological time that their stability becomes a paradox in a world of Darwinian evolutioanry flux and continuity. As a double irony -- see pages 817-820 for a full discussion in the light of punctuated equilibrium's different reading -- we have also thoroughly misinterpreted this phenomenon under the same gradualistic bias that inspired our notice in the first place! The classical "living fossils" (the inarticulate brachiopod Lingula, the horseshoe crab Limulus polyphemus, the extant coelacanth) are not long-lived as species (Limulus polyphemus, for example, has no fossil record at all), but rather belong to clades with such a low speciation rate that little raw material for cladal trending has been generated over the ages.)(Gould 2002:937, and yes, it's an entire parenthetical paragraph)

One may immediately object that the lack of fossil evidence does not establish that a species is not "long-lived", in terms of its duration. It does, however, compromise the ability of such a species to be evidence of stasis -- just as the lack of a chimpanzee fossil record reduces their ability to inform us about the chimpanzee-human common ancestor.

But here, Gould was on to something that is relevant to me, so I read on. The passage was an extended aside in a section concerning the interpretation of trends as differential survival of species within clades (thus, "cladal trending"). As cited here, the idea was introduced earlier in the book.

Here are some relevant parts of pages 817-820:

Paleontologists had been truly stymied in their thinking about the important and contentious topic of "living fossils." Neither of the two conventional explanations could claim any real plausibility. Every textbook that I ever consulted as a student dutifully repeated the old saw that living fossils had probably achieved optimal adaptation to their environment. Therefore, no alternative construction could selectively replace an ideal form achieved so long ago. But no one ever presented any even vaguely plausible evidence for such a confident assertion. Why should horseshoe crabs lie closer to optimality then any other arthropod? What works so well in the design of lingulid vs. other brachiopods? What superiority can a lungfish assert over a marlin or tuna? In fact, since living fossils also (by traditional depiction) present such a "primitive" or "archaic" look, the claim for optimality seemed specially puzzling.
The other obvious explanation, in a gradualistic and anagenetic world ruled by conventional selection, held that living fossils had stagnated because they lacked genetic variation, and therefore presented insufficient fuel for Darwinian change. This more plausible idea seemd sufficiently intriguing that Selander et al. (1970), in the early days of electrophoresis as a novel method for measuring overall genetic variation, immediately applied the technique to Limulus, the horseshoe crab -- and found no lowering of genetic variability relative to known levels for other arthropods. This negative pattern has held, and no standard lineage of living fossils exhibits depauperate levels of genetic variability (Gould 2002:816).

Gould here didn't acknowledge the import of the neutral theory upon this particular electrophoretic result. Almost all of the standing genetic variation in every species is neutral or very nearly so; adaptive variation either is in selective balance or is highly transient. The standing electrophoretic variation within a species is next to irrelevant to its evolution, except in certain limited cases where neutral variation has been highly restricted.

The question is not whether a species has any genetic variation, but instead whether it has been presented with adaptive genetic variation at any substantial rate (say, equal to that of other species). If a species is locked within a single ecological niche for a long time, it is easily imaginable that the appearance of new adaptive genetic variants should be very, very, very rare. This of course converges on the first explanation, that any species with such a long duration must be very near optimality.

So, what is Gould's alternative?

But punctuated equilibrium suggests another, remarkably simple, explanation once you begin to think in this alternative mode -- an insight that ranks in the exhilarating, yet frustrating, category of obvious "scales falling from the eyes" propositions, once one grasps the new phrasing of a basic question. If evolutionary rate correlates primarily with frequency of speciation -- the cardinal prediction of punctuated equilibrium -- then living fossils may simply represent those groups at the left tail of the distribution for numbers of speciation events through time. In other words, living fossils may be groups that have persisted through geological time at consistently and unvaryingly low species diversity. (Average species longevity need not be particularly high, for low species numbers, if consistently maintained without geological bursts of radiation, will yield the full effect.) Such groups cannot be common -- for consistently low diversity makes a taxon maximally subject to extinction in our contingent world of unpredictable fortune, where spread and number represent the best hedges against disappearance, especially in episodes of mass extinction -- but every bell curve has a left tail (Gould 2002:816-817).

The next few pages detail the case of the lungfish, which is a well-studied lineage. In abstract, shortly after the first fossil appearance of lungfishes, there were a great diversity of species. Later this diversity greatly declined. During the period of time when lungfishes were diverse, their rate of morphological evolution was high. During the long period of subsequent time when there have been few lungfish species, the rate of morphological change was very slow. The example is drawn from Westall (1949), which is reproduced in many paleontology texts.

Gould asserted that this relationship is a causal one. Early in the evolution of lungfishes, a high rate of speciation caused a high rate of morphological change. Later, morphological change was impossible because of a low rate of speciation.

Why did Gould render this apparent association as a causal one? Because he thought that morphological change was mainly caused by speciation. In his opinion, phyletic evolution within species is rare. If morphological change is unlikely in the absence of speciation, then the absence of speciation must result in no significant morphological change. QED.

But this circular account leaves a couple of threads dangling, and a good tug to one or the other causes the circle to unravel.

First, is the amount of phyletic evolution expected to be zero or nonzero? Gould's explanation for living fossils would appear to work only if there is no possibility of phyletic evolution at all. Why? Because if some phyletic evolution is possible, then the hundreds of millions of years during which "living fossils" have persisted should have generated substantial evolutionary changes. But the lack of substantial change is exactly what "living fossils" are supposed to demonstrate. Gould asserts that this lack of change is the expected result of stasis in the absence of speciation, "stasis" meaning "no phyletic evolution."

What exactly explains this extraordinary evolutionary stasis? Gould lists several possible mechanisms for stasis on pages 877 through 885. Although he lists "stabilizing selection" as one of six possible mechanisms, in truth all six of these "mechanisms" rely on stabilizing selection to explain the lack of change.

But wait a minute. If stabilizing selection, in one form or another, is ultimately responsible for stasis, then a static species must stay the same because its fitness is maximized. (This makes implicit sense, since if its fitness wasn't maximized, it would necessarily change!). But doesn't that imply that this unchanging species is, in fact, optimally adapted to its environment?(*) Gould's "scales falling from the eyes" hypothesis seems to have led us right back to "that old saw" about optimal adaptation! The circularity was entirely a detour from the real explanation.

Second, why was lungfish diversification in the past so much higher than it has been more recently? For Gould's explanation to hold much weight, the rate of speciation in living fossils must somehow be constrained by factors intrinsic to these species. Why intrinsic? Because if the living fossils were constrained by extrinsic factors, then these same extrinsic factors could more simply explain long-term stasis without recourse to speciation rate.

Consider a traditionalist explanation for the lack of present-day lungfish diversity: ecological constraint. Lungfish do not speciate extensively today because the potential ecological space for them is already occupied by species that are well adapted to it -- at least, well-enough adapted to repel the incursion of transitional lungfish. Bluntly, lungfish cannot invade the land and become fully terrestrial because there are plenty of terrestrial species that would eat them for lunch. Likewise, they cannot grow much larger because other large fish species (or in some instances, crocodiles) already do a good job of it. And so on.

Earlier in lungfish evolution, things were different. Many of the spaces now filled by other species were open and available for the new lungfish lineage. The reduction of the lungfish diversity was caused by the increase in diversity of competing taxa from other clades. The outcome of this ancient competition may have been decided by any number of factors, including intrinsic disadvantages of lungfish body plan compared to other fish or tetrapods, greater adaptability of other clades, or simple bad luck. But the species of lungfish that remain are the ones whose niche was exceptionally resistant to invasion by species from other clades, because they exploit the unique adaptations of the lungfish themselves. This account may not be complete, but it illustrates a conventional evolutionary approach.

Notice in this scenario that lungfish diversification is entirely a function of extrinsic influences: the availability of ecological space, the presence of competitors, the effects of ancient happenstance. I invoked these factors to explain the lack of species diversity of the lungfish clade.

But notice that these extrinsic factors are precisely the same ones that would explain long-term stasis of lungfish. And, in fact, the explanation of low diversity is entirely incidental to the explanation of stasis. The presence of competitors, the effective adaptation to their ecology, and good luck explain why lungfish have not changed as extensively in recent time.

This would be true no matter how many species of lungfish there are now. Consider sharks, another "living fossil" in a sense, but a highly speciose clade. Or crocodilians. Or chelonians. These are all clades that have maintained a consistent morphological pattern through at least the past 100 million, and generally the past 200 million or more years. Today they are diverse clades, but their major features were established early in their evolutionary history -- especially in contrast to more recently emerging groups, like mammals and birds.

If the usual extrinsic factors are the explanation for low speciation rates in lungfish, then they are also the explanation for stasis. There is no need to posit low speciation rates as an intervening cause -- and indeed, the example of relatively static clades with high speciation rates gives the lie to Gould's chain of causation.

Are there any intrinsic limits on speciation in lungfish? Unlike some other examples that Gould uses in his discussion of species and clade selection, lungfish do not have low reproductive rate, and it's not obvious that they lack the ability to colonize new habitat. But more directly, lungfish had a high speciation rate early in their evolution. This early diversity shows that lungfish are not intrinsically constrained in their speciosity. Instead, it is the extrinsic factors that have limited both lungfish evolution and diversification recently.

Again, the explanation for stasis is stabilizing selection in one form or another. Again, we are back to the "old saw" of optimal adaptation.

Gould's story about "living fossils" is, then, nothing more than a massive distraction. What makes lungfish different from marlin or tuna is their ecology. Their speciosity is a side effect, not a cause.

Notes:

*Of course, maximal fitness and optimal adaptation are not the same thing. In particular, maximal fitness in a population implies only that the current alleles are at optimal frequencies, not that the population has necessarily evolved as far as it will go. Nevertheless, a population that has oscillated near maximal fitness for a few million years has got to be as close to a description of “optimal adaptation” as anyone is likely to find. </p>

The operative problem here seems to be an ambiguity about the meaning of "optimal". For example, the adaptation of any species can easily be shown to be less than optimal, if a better competitor can be introduced in its habitat. Thus, thylacines may have been optimally adapted predators in the prehistoric Australian context, up to the point that humans and dingos arrived to compete with them. But if by "optimal" we mean "better than any conceivable competitor", it is pretty likely that no species can ever be "optimal". Thus, a sensible application of "optimal" would apply to the possibility of change within the species itself: if no further change is possible given the selective constraints at work, the species' adaptation is fairly said to be "optimal". In this sense, an "optimal adaptation" is one in which further increases in fitness are either impossible or are exceedingly rare.

It is this ambiguity in the term "optimal" that Gould exploits in his hypothetical comparison of lungfish to marlin and tuna. What do lungfish have that marlin and tuna lack? Their environment, of course.