The Devil Ray's in the Details

So mantas aren't a thing anymore... - paraphrase, David Shiffman's liveblog of my talk at the recent meeting of the American Elasmobranch Society.

Wow, is that going to require some explanation! Did I steal these guys away under cover of night? Did they pull a "so long, and thanks for all the fish" on us? No, this is a story about the power of naming, and one that may have serious implications for the conservation of these amazing animals and their close relatives.

Human beings love to name things. We do it vigorously and redundantly: a single fish species may be christened with a dozen or more common names by people in different geographic areas, times, or even marketing departments! It helps to have an international-standard system of naming animals to give this enterprise some consistency. It doesn't matter if you know it as Chilean Sea Bass or the Patagonian Toothfish, people worldwide will be happy to confirm for you that Dissostichus eleginoides is indeed one ugly customer.

This system of precise identification in which scientists apply a formal code to name organisms is called binominal nomenclature ("two-part name"). This is often incorrectly called "binomial" nomenclature ("two number," a mathematical expression), even by professionals! The first part of the name is the genus, which can apply to between one and many species that are closely related and resemble each other. The second part of the name is the specific epithet, which applies to one and only one species. These names are usually derived from Greek and Latin. For example, Batrachognathus volans translates as "flying frog-jawed" one, an apt appellation for an odd pterosaur from the Late Jurassic.

A genus (plural genera) should describe some small set of similar organisms. This group should be defined by a common ancestor, all of its descendants, and nothing else (Figure 1A). We call these natural groups, or clades.

This is the ideal case. What happens if you end up with something like Figure 1B? Here, you can see that one genus is "nested" inside the other one: Mobula is not a natural group because it inappropriately excludes Manta. It's easy to analogize this to how, in some cultures, family names are passed down the paternal line. If you, your father, his father, and all male relatives in between are named "Lannister" but one of your brothers is named "Baratheon," something's gone wrong in the process of naming!

Under the current classification scheme, there are two genera of "devil rays": two species in the genus Manta and nine species in the genus Mobula. Besides some slight differences in body proportions, there are a few characteristics that distinguish Manta from Mobula. Most notably, Manta lack teeth on the upper jaw and have a mouth at the end of the head, while the mouth of Mobula is underslung as in most sharks. In recent years it has usually been held that the classification of devil rays is a valid arrangement, following Figure 1A.

However...

Evidence from both DNA sequences and comparative anatomy suggests that current devil ray classification actually fits Figure 1B, making it invalid.

DNA sequence analyses from my doctoral dissertation work ^[1], followed by a large-scale study performed by my graduate advisor and colleagues ^[2], suggested that Manta is nested within Mobula. While not all species were sequenced, Manta birostris was indicated to be more closely related to Mobula japanica than it is to other sequenced Mobula. This is based mostly on evidence from one or two genes, with a couple of others rather uninformative. It was compelling enough to get me to delve back through the scientific literature on the anatomy of the group, and what I found was surprising.

It turns out that biologists who have taken a close look at devil ray anatomy have been quietly suggesting for nearly 15 years that Mobula is not a natural group! ^[3,4] For example:

 • Most devil rays have comb-like teeth, while Manta, Mobula japanica, and Mobula mobular have distinctive peg-like teeth. ^[3,4]

 • Mobula japanica (>3m wide) and Mobula mobular (>5m?) are among the largest devil rays, comparable in size to the recently described Manta alfredi. ^[5,6]

 • Among devil rays, only Manta, Mobula japanica, and Mobula mobular have caudal spines (the "sting" in "stingrays"). ^[5,6]

So is this enough to overturn the current system of classification for devil rays? Not yet. If any changes are to be proposed, someone first needs to perform a formal "taxonomic revision" of both Manta and Mobula. This means that they need to present a sound, peer-reviewed case for the reclassification of these species, which will require physically re-examining them and ideally presenting corroborating DNA evidence. This must include the "type species" for each genus: Manta birostris and Mobula mobular. A type species is the one to which the name of the genus is permanently attached; in this case, it defines "what a Mobula should be." There are to date no available DNA sequence data for Mobula mobular, although we can predict that they will group most closely with Manta and Mobula japanica.

Assuming the evidence continues to build that Manta is nested within Mobula, what happens next? The most likely case is that the genus Manta will cease to be valid, subsumed under Mobula as a "junior synonym." Mobula has precedence under the rules since it was described in 1810, versus 1829 for Manta. There are mechanisms by which a name can be suppressed: the proposed renaming of the fruit fly species that's the cornerstone of much of modern biology would be a nightmare beyond measure (see here), but Manta is unlikely to qualify. Their common names will remain "Manta Rays" and the world will go on turning. Given the scarcity of materials from some species and their often colossal size, I don't envy the gal/guy to undertake the formal review of the devil rays... but it needs to be done. Five bucks says that Manta is going away in the next ten years.*

So why does this matter? Legal issues and conservation.

Savvy folks sitting in the conference room or reading David's liveblog quickly seized upon this question. With Manta recently receiving protection under the Convention on International Trade in Endangered Species (CITES), would lumping these guys in with Mobula expose them (1) under a legal technicality and/or (2) as less unique and worthy of conservation than when they had their own genus? Fortunately, shark conservation experts including Sonja Fordham (President at Shark Advocates International / Deputy Chair at IUCN Shark Specialist Group / conservation rockstar) were on hand to address these concerns.

Fears of CITES loopholes appear to be unfounded. Current protection schemes are thought to be engineered to continue to protect the two named (plus a third suspected but undescribed) species of Manta. Prying at loopholes is sadly unnecessary: countries that would otherwise seek to do so can apparently just opt out of CITES protections (I am aiming an unimpressed glare squarely at you, Canada and Guyana).

In short, this is less a threat to mantas than it may be an opportunity to extend protections to the other devil rays. Most of these species are heavily affected by both targeted fisheries and as bycatch, but they exhibit human-like life histories that make them extremely vulnerable to such pressure. Despite this shared and imminent danger, only Manta - with its tremendous charisma - seems to have found many champions in conservation, evidenced by the fact that only Manta species were proposed for CITES listing. Changing its name won't make these folks give up the cause, but folding all of the devil rays into a single genus can underscore the similarities in vulnerability across species in this group, strengthening the case for offering them equal safeguards in the future.

"Mantas aren't a thing anymore"? Sounds good to me.

*Offer valid for first claimant as of ten years from the date of this article's publication. If I win, I'll pick one of you at random and demand my fiver.

References
¹ Aschliman NC (2011) The batoid tree of life: recovering the patterns and timing of the evolution of skates, rays and allies (Chondrichthyes: Batoidea). Dissertation, Florida State University
² Naylor GJP, Caira JN, Jensen K, Rosana KAM, Straube N, Lakner C (2012) Elasmobranch phylogeny: a mitochondrial estimate based on 595 species. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives, 2nd edn. CRC Press, Boca Raton, Florida, pp 31-56
³ Herman J, Hovestadt-Euler M, Hovestadt DC, Stehmann M (2000) Contributions to the study of the comparative morphology of teeth and other relevant ichthyodorulites in living supra-specific taxa of Chondrichthyan fishes. Part B: Batomorphii 4c: Order: Rajiformes - Suborder Myliobatoidei - Superfamily Dasyatoidea - Family Dasyatidae - Subfamily Dasyatinae - Genus: Urobatis, Subfamily Potamotrygoninae - Genus: Potamotrygon, Superfamily Plesiobatoidea - Family Plesiobatidae - Genus: Plesiobatis, Superfamily Myliobatoidea - Family Myliobatidae - Subfamily Myliobatinae - Genera: Aetobatus, Aetomylaeus, Myliobatis and Pteromylaeus, Subfamily Rhinopterinae - Genus: Rhinoptera and Subfamily Mobulinae - Genera: Manta and Mobula. Addendum 1 to 4a: erratum to Genus Pteroplatytrygon. Bull Inst R Sci Nat Belg Biol 70:5-67
⁴ Adnet S, Cappetta H, Guinot G, Notarbartolo di Sciara G (2012) Evolutionary history of the devilrays (Chondrichthyes: Myliobatiformes) from fossil and morphological inference. Zool J Linn Soc 166:132-159
⁵ Notarbartolo di Sciara G (1987) A revisionary study of the genus Mobula Rafinesque, 1810 (Chondrichthyes: Mobulidae), with the description of a new species. Zool J Linn Soc 91:1-91
⁶ Marshall AD, Compagno LJV, Bennett MB (2009) Redescription of the genus Manta with resurrection of Manta alfredi (Krefft, 1868) (Chondrichthyes; Myliobatoidei; Mobulidae). Zootaxa 2301:1-28

Photos from Wikimedia Commons
Manta: LINK
Mobula: LINK

Shattering the Vegetarian Myth: Meat Consumption Was Intrinsic to Human Evolution

Apologies for the absence. It takes time to finish one life and start another.

At least this dragged me back into the scene: Kathy Freston's "Shattering the Meat Myth: Humans Are Natural Vegetarians." The piece is, and I hesitate to write this in an age where one's Google News feed bears a striking resemblance to The Onion, a breathtakingly poor scrap of doggerel. Even for ill-researched propaganda, this beast is remarkable in its reckless and wanton distortion of not only science, but of history as well.

This rebuttal in no way touches upon the relative morality or nutrition of diets that include or exclude animal products. In fact, the article came to my attention via Facebook by a respected friend and colleague who takes a valid moral stance against meat consumption. However, with 20,000 other Facebook Likes at the moment, I cannot let the grotesque inaccuracy of the arguments from biology stand. To crib from Samuel L. Jackson's character in Pulp Fiction, "Well, allow me to retort!"

Freston argues as follows (and by all means, read the original to evaluate my summary).
1. The inclusion of meat in the human diet is a product of agricultural civilization (circa 10,000 years ago) and is incompatible with a plant-based biochemistry that dates back "at least tens of millions of years." Prior to the rise of herding, "we may have needed a bit of meat… in times of scarcity."
2. "Humans are herbivores" because we lack physical adaptations that make it easy to tear flesh and hide, such as overdeveloped canine teeth and claws. We resemble the other great apes in that we process food with our hands and must have similarly had "a largely plant-based diet."
3. Humans have "never adapted" to a meat-inclusive diet because meat-eaters have a higher incidence of heart disease, cancer, and diabetes.

Freston's deeply flawed arguments can be attacked from historical, evolutionary, and logical angles. Let's get the observed history out of the way so we can get on to the evo.

A History of Meat Consumption
Let us assume, for the purposes of clarity (since Freston surely provided little), that the "natural" state of humanity refers to traits expressed prior to civilization and its concomitant horrors. Freston has asserted that, before the advent of agriculture-dependent herding 10,000 years ago, humans consumed only small quantities of meat in times of hardship.

Um. But.

This ignores the physical record of at least 70,000 years of hunting. Hunting big things. From some of the earliest human art on cave walls depicting the hunt, to no shortage of archaeological sites riddled with thousands of mammoth bones (one example), remains of other large and small mammals, deep middens of fish bones and mollusk shells, and so on. By about 10,000 years ago, we were in part responsible for the disappearance of nearly every large mammal in the Western Hemisphere by eating them toward extinction.

South African cave art. Photo Credit San Felszeichnung, from Wikimedia Commons.

Of course, then civilization struck and, well… a grand total of zero of the remotely successful cultures on the planet, now or in recorded history, have categorically excluded meat from their diet. Jared Diamond has a little more to say on the subject.

But let's throw Freston a bone (hah) and examine her argument in the time frame of millions of years. What does biology have to say?

Pretty Much The Same Thing
Freston views humanity through the lens of our closest living relatives, the other great apes, so let's follow. Our sister group, the two chimpanzee species, eat lots of lovely fruits and vegetable bits. Er, and also insects, birds, and mammals including other primates and small relatives of cows and pigs(!). Meat only comprises about 5% of their caloric intake, but for a species relying on its hands, primitive tools and wits, it's seriously impressive that they can muster as much.

Is Freston correct that the human gut tract is like the intestines "of other herbivores" in being very long? No, we're rather intermediate on the spectrum between hypercarnivores and herbivores. Incidentally, carnivore gut tracts are not particularly short "so they can quickly get rid of all that rotting flesh they eat" - another of the bountiful instances in which Freston's sensationalism throws science on the fire. Carnivores have a short and efficient intestinal tract in that they don't need to process large quantities of generally indigestible plant fibers. Our barrel-shaped rib cages, rather than the conical arrangement exhibited by primates that consume more plant matter, in part reflects this reduction in gut length.

Freston laments the absence of wicked claws and fangs (actually, in primates the size of the canine teeth is strongly correlated with social structure rather than with diet) and such. If only humans had a way of compensating for that!

Oh. Right. The whole running and tools thing.

A proper treatment is well beyond the scope of this post, but the evolution of the human body plan from that of a four-footed ancestor appears to have been driven in large part by selective pressure on the ability to run long distances efficiently - and later, while holding tools. Our legs and feet are superbly adapted to long distance running. The NYT has a decent, if brief summary of a few of these characters, and there's a skeletal outline of the endurance running hypothesis over at Wiki. This ability may be nearly 2 million years old, dating back to Homo erectus.

There are a couple reasons for us to run long distances: to poach kills (in fact, that's how we got tapeworms from large cats and hyenas), and to run prey into the ground. Turns out we're pretty good at that (awesome Attenborough video!). We run, we track, and unlike many of our large prey, we can sweat to cool off in the chase. Persistence pays off.

Might meat consumption have put evolutionary pressure on not only our body plans, but on our developmental timing as well? Humans wean their offspring at a very early age relative to other great apes (2 years and change in humans / 5 in chimps / 7 in orangutans, which consume very little animal protein). This is a pattern common to carnivorous mammals (PLoS ONE original). Carnivores wean their offspring faster than do herbivores due to improved milk quality and/or the ability of the offspring to eat high-energy meat. After weaning, females again become receptive to mates; the upshot is that a shorter weaning period increases reproductive capacity.

The preponderance of evidence suggests that Freston's thesis could not be more wrong. The increased means to acquire and utilize meat was likely one of the major driving forces behind the evolution of our bipedal body plan optimized for endurance running, our ability to make and manipulate tools, and our developmental timing. There are other human relatives that were more clearly geared toward eating tough plant matter. They didn't make it.

But It'll Still Kill You
Meat is an extremely efficient source of nutrients, including proteins, fats, vitamins, and minerals. When combined with leafy greens and other nutritious foods and an active life style, it helps build healthy bodies. In the short term. In the long term, the consumption of, in particular, red and processed meats is linked to increased risk of cardiovascular disease, certain cancers, and diabetes.

Apparently needing a screamingly ludicrous sound bite from an otherwise distinguished individual, Freston concludes her sad crusade with this gem from Dr. William Roberts, editor of the American Journal of Cardiology. In its entirety: "Although we think we are, and we act as if we are, human beings are not natural carnivores. When we kill animals to eat them, they end up killing us, because their flesh, which contains cholesterol and saturated fat, was never intended for human beings, who are natural herbivores." Coupled with another MD suggesting that "our bodies have never adapted to [eating meat]," it begs the obvious question: why did our ancestors eat meat - and as we have seen above, they certainly did - if it predisposed them to disease? The answer, again, rests in timing.

Except in cases of gross excess and sedentary life styles, these pathologies tend to strike late in life. Specifically, they largely affect post-reproductive (or nearly so) individuals. If you die at 55 from a heart attack but raise ten vigorous, meat-fed offspring, you still have dramatically higher fitness than a vegetarian who lives to 90 but raised five offspring before menopause. Additionally, during the course of human history, "post-reproductive" is a luxury that an incredibly small portion of the population would ever live to see; those disorders would be invisible to natural selection. The MDs' argument is completely vacuous. While they may mean well, I won't stand by to see them misinform the public in order to do so.

It's good to be back.

[Note: Desmond Morris tackled the evolution of humans as a balancing act between carni- and herbivory in his classic The Naked Ape.]

A Day Late and a Dollar Short

Please forgive the absence. June was spent running analyses and putting together my talk for the Joint Meeting of Ichthyologists and Herpetologists (nerds working on fishes and reptiles/amphibians, respectively) in Providence. Two glad tidings: I have returned to wax scientific on subjects, and I was honored to receive the ASIH Stoye award in General Ichthyology at the conference. Before the year is out, I will write an article here on the same: what the interrelationships of batoid fishes, my study group (skates, rays and allies), can tell us about widespread convergent evolution and the effects of the end-Cretaceous extinction event on their current patterns of diversification.

Speaking of mass extinction...

This one has been a while coming. Toward the end of last year, several science news outlets picked up a striking article in the journal Biological Conservation. In short, it suggested that current guidelines for setting minimum population sizes for protected species, like the black rhinoceros, are at least an order of magnitude (10x) too low to adequately protect them from extinction in this century. The current guidelines adhere to a "50/500" rule, in which a minimum of 50 adults are required to avoid the negative effects of inbreeding, and a minimum of 500 to be able to adapt to long-term environmental changes or rebound from a catastrophic event.

Ten times too low. Put a big, flashing exclamation point at the end of that one. Horrifying corollaries are immediately evident: many species are already too far gone to be preserved in the long term even if we dropped everything to triage them now, and species we think we've done a bang-up job of protecting to date may just need one calamity to drop them below that point of no return. In light of the political difficulties - an understatement by any measure - of maintaining even today's meager/modest conservation measures, a tenfold increase will never happen. These species, humble to majestic, mountain gorilla (~400) to desert pupfish (42!), are going away sooner than we'd like.

It is not an encouraging picture.


Black rhinoceros. Photo credit John and Karen Hollingsworth, USFWS, from Wikimedia Commons.

This is not a political blog, so we'll leave the issue behind and look at what these numbers mean. Why do we need X number of animals to avoid catastrophe? The first barrier, inbreeding, is intuitively obvious: offspring are produced by close genetic relatives. Put another way, the two copies that an individual carries of each her genes have a high probability of being identical by descent, or having come from the same ancestor (grandma) independently through each parent. Gross, yeah. But why is this necessarily a bad thing? Every human has two identical copies - alleles - of at least some genes, and we're not all running around with horrible genetic abnormalities. Things go south (no pun intended; I am from Texas after all) when you deal with genes that have a healthy version and a defective one.

At many gene locations in your DNA, you have one healthy allele and one defective one. In most cases, the normal copy steps up and does a stalwart job compensating for the freeloader. You'll never notice that one copy is bad, and so we call that copy a recessive, or hidden allele. That's the good news. The bad news is that they're ticking time bombs on a generational timescale. When you reproduce, one of those alleles is "drawn" at random to end up in your sperm or eggs. If you pass on the healthy version, great, your child will be A-OK for that gene. If not, you'd better hope that your mate contributes a healthy copy to pull the weight for your freeloader. If two recessive alleles end up in the offspring, she won't be able to make that gene's normal protein product. The effects may be mild, and even desirable to some: blond hair or blue eyes. Or instead, they may cause a serious genetic malady like cystic fibrosis or sickle cell anemia. If you have one healthy and one hidden, defective allele for a disease-associated gene, you are a carrier. Everyone on the planet is a carrier for an unknown, but probably not inconsiderable, number of genetic disorders. This is the basis behind genetic testing, which is becoming cheaper and more widely available every year.

The rest is easy to follow. If you're a cheetah and there are only a handful of your species left (the cheetah-reality is not that dire), the odds that you are closely related to any other cheetah you see are much higher than they are for a species with larger population sizes, like industrialized humans. If you mate with that cheetah, your odds of having the same set of alleles from a common ancestor are high, and an increasing proportion of offspring will either have two healthy or two defective copies of a gene - allele fixation. You can see how the situation degrades quickly once disease traits become universal in a population. Lost genetic diversity takes a long, long time to be recovered.

The second, higher requirement for a minimum viable population size (the 500 of the 50/500 rule) is trickier to understand. It builds on the concept of inbreeding, but the higher number of organisms keeps a larger gene pool - the total genetic variation in a population - available into the future. High genetic variation gives a population options, so to speak, in the face of environmental change. There may be warmer-adapted cheetah alleles that would do better under increased temperatures, or slightly faster cheetahs that can better keep up with Thomson's gazelles, which are under similar pressures. Perhaps most importantly, it provides options for [pathogenic] disease resistance.

Viruses, bacteria, and other parasites are engaged in a constant arms race with their hosts at a molecular level. Genetic variability goes a long way to ensure that at least some cheetahs will survive a potent disease, while if they are genetically homogeneous, a single bacterial strain that has "figured them out" can wipe out the whole population in one fell swoop. As a great recent example, humans of European descent have a much higher incidence of a genetic mutation called CCR5-delta32 that provides resistance to HIV. This mutation also appears to confer resistance to the great historical European plagues. That is, some Europeans had this mutant allele and became resistant to plague, while other didn't and were selected against. If Europe's population had been much smaller, this mutation may have never arisen and the entire continent could have been taken out in one of those dread epidemics.

A grim picture, to be sure. The next steps are political, but having been introduced to the science, hopefully you are in a better position to weigh the costs and benefits of conservation measures for yourself.

Here's to an educated democracy.

This reView of Life(?): Viruses, Part 2

The first decade of this brave new century was characterized by dramatic upheavals, often violent, in politics, business... and film. Perhaps through widespread disillusionment in the wake of crises in security and finance, perhaps merely the pendulum swinging back from the fantastic (read: "divorced from reality") flavors of storytelling in the 1980s - early 90s, the public has rushed to embrace the gritty and believable. Joel Schumacher's candy-colored Batman films were usurped by Christopher Nolan's dark masterpieces, achieving almost ridiculous commercial success. Peter Jackson breathed life into a vision of The Lord of the Rings that eschewed most of the magic and occasional levity of the book, and also featured a rather mundane, if attractive, aesthetic. Additional existing franchises and concepts from other media leapt to the big screen or were rebooted, and surprisingly often attempt to feature some "scientific" hook to enhance the believability of the tale. One of the rising stars of this movement is our enigmatic acquaintance, the virus.

Viruses are now almost universally implicated as the nefarious causal agent in modern zombie tales or close cousins, such as the animalistic, deranged "infected" in 28 Days Later. Alas, the point of this article is not to tackle the questionable physiology of a zombie (actually, that sounds like a good one for another day), but rather to touch on Hollywood's mixed success in portraying the pathology of viruses.


The virus in 28 Days Later is particularly terrifying in that, 30 seconds after exposure, a victim is reduced to a hemorrhaging, raging volcano of virus-laden fluids. One infected person in a crowd can effect some sick parody of The End Times in mere minutes. Viruses in many other films spread with similar urgency, in some cases reanimating a corpse within two minutes of exposure (Dawn of the Dead reboot). What does the real world have to say about this?
©2002, 20th Century Fox.

Viruses are constrained by the same physical laws that the rest of us are, regardless of your definition of "life." A generic viral life cycle, and there are all sorts of bizarre variants, goes something like this:
 1) find a host cell;
 2) enter the host cell, or inject genetic material;
 3) use own or hijacked machinery to replicate genes and coat proteins;
 4) stay forever, or have all your copies erupt out of the host cell;
 5) repeat.

Each of these steps requires time, particularly step (3). This is even more of a problem for related scifi concepts involving rapid gains of animal/plant/fungal tissue, or what I call "The Werewolf Problem." I'll leave that for another day.

The window of time between initial exposure and the point at which symptoms first emerge is called the incubation period. During incubation, viruses are reproducing and spreading through host cells but are at insufficient numbers to make much of an impact. Yet. So how long is this timetable? Clearly 30 seconds for complete system takeover is unrealistic.

The fastest acting human virus, as far as I have been able to discover, is the stringy little fiend below, ebola. The incubation period of ebola is 2 - 21 days, but usually 5 - 18 [source: Emerging infectious diseases 9(11):1430-7; via Wikipedia]. The fastest.


Ebola virus. Photo Credit Centers for Disease Control, from Wikimedia Commons.

A common pattern of viral strategies is a correlation between their agressiveness and their ability to be transmitted. Ebola and similar viruses have evolved a strategy that is very much living (yes, I said it) on the edge. They emerge, spread and kill so quickly that they run the risk of not being able to find a new host and suffering local extinction. Compare this to the less common strain of the virus that causes AIDS, HIV-2. HIV-2 often degrades the immune system more slowly than does HIV-1, leading to higher long-term survival rates. It also is less successful at being transmitted between people. For an analogy in honor of the ongoing NBA finals, it may only shoot 60% from the field compared to HIV-1's 80%, but gets an extra five minutes of playing time. The natural world is full of these trade-offs, in which organisms fine-tune their life strategies over time.

The ones that fail? Well. We don't see those guys anymore.

On that note, next time I will likely bring up some recent, distressing speculations about the fates of endangered species.