Turtles and long branch attraction
I. Sauropsid Phylogeny: All organisms more closely related to crocodylians and lizards than to Synapsids.
II. Anapsida. This group contains a number of distinct fossil groups. Our resaons for covering them here will become apparant soon. The etymology comes from the anapsid condition of the anapsid skull. Yet, like egg-laying in monotremes, this is a plesiomorphy, not a synapomorphy.
- The pattern: All amniotes that are not synapsids are sauropsids. All of this diversity breaks down into two large groups, Anapsida and Diapsida plus a few small fossil ones.
- Synapomorphies include:
- Openings in palate beneath orbits.
- Color vision.
III. Diapsida: This is a very diverse group, both in living and fossil members. In this lecture we only begin to acknowledge its diversity.
- Synapomorphy: Occipital condyle (the knob by which the skull articulates with the vertebral column) markedly posterior to jaw articulation.
- Anapsid diversity. Although there was a great diversity during the Late Paleozoic and earliest Mesozoic, we focus on two major examples.
- Proportions: Generally small, squat, robust reptiles, some superficially resembling horned lizards.
- Teeth: They had blunt, strong teeth, presumably for processing plant material.
- Armor: Some members had dermal armor plates in skin.
- Fossil record: Late Permian to Late Triassic.
- Proportions: Medium to large herbivorous reptiles. Short, deep and wide bodies, presumably with large digestive systems.
- Teeth: Teeth are leaf-shaped teeth, similar to those of herbivorous large iguanas.
- Armor: Pareiasaurs have extensive dermal armor. In some, the armor is interlocking. Thus, everything points to these creatures having been large, slow moving armored herbivores with extensive digestive systems.
- Fossil record: Restricted to the Late Permian.
IV. Testudines. Living turtles and their close fossil relatives.
- Synapomorphy: Diapsid condition of skull, with infratemporal fenestra (independently derived from that in Synapsida) and supratemporal fenestra, a completely new feature.
OK, that was all to set up the context. Now comes the real issue.
- There are a number of primitive "stem-diapsids." They are related to, but outside of the crown group.
- Sauria: Within Diapsida is a crown group defined as the most recent common ancestor of living lizards and crocodylians, and all of its descendants.
- Lepidosauria: Another crown group - The most recent common ancestor of living lizards and Sphenodon (the New Zealand tuatara), and all of its descendants.
- Archosauria: The most recent common ancestor of living crocodylians and birds, and all of its descendants.
V. Follow the bouncing turtles: But, what we haven't covered is where turtles fit into the vertebrate tree. Of all current phylogenetic enigmas, this one is probably the most intractible.
- Shell, combining elements of the axial skeleton and dermal plates. On top of this shell skeleton is a series of large scales that do not match up with the underlying bones.
- Loss of teeth. In turtles, the mouth is lined by a horny beak made of keratin, like a bird or dicynodont beak.
- The synapomorphies of this group barely begin to encompass their wierdness. Indeed, if turtles were only know from fossils, people would stream into museums to see them. Some aspects of turtle wierdeness:
Confirmation of evolution. Biologically turtles illustrate a fundamental fact about evolution - Life span is correlated with your ability to avoid accidental death.
- In all other vertebrates, the appendicular skeleton is literally appended to the axial skeleton. Among turtles, and only among them, the axial skeleton has grown around the appendicular skeleton - the limbs and limb girdles. This represents a major tweaking of their developmental pathways.
- The shell of a turtle is functionally different from that of an animal like armadillo in that it is completely inflexible and encompasses the torso in one solid unit. This creates a number of biological challenges. The biggest one is breathing. A normal amniote moves air into and out of its lungs by expanding and contracting its ribs. (More on that later.) In turtles, this is impossible because the ribs are part of the solid and inflexible shell. Instead, they change the volume of their chest cavities by pumping their limbs in and out.
- Turtles, like synapsids, use an impedance-matching ear. In turtles, however, the tympanum is not supported by post-dentary jaw bones. Rather, it is supported by the quadrate, which has a deep posterior embayment.
Suppose that humans have a variety of genes, some of which confer an advantage for individuals above age 150 and some that are lethal for people that age, but that don't effect younger people. Can natural selection select for the advantageous gene? No, because it never gets the chance. People don't live that long. Indeed, for all critters, natural selection for mechanisms of self-repair of the body can only work if at least a few individuals are still alive and mating at the age when this would be an issue.
Animals like marsupials are usually dead from predation, disease, or accident before they reach this point. But what happens with animals that posess some adaptation that keeps them relatively safe? These may reach advanced ages where natural selection can work on mechanisms for body repair - i.e. longevity. For this reason, when you compare mammals and birds of similar size, the birds almost invariably have the longer life span. But they can't compare with turtles. These creatures, in natural settings, at least, are so immune to predation and accident that they have evolved extreme longeivity. Indeed, it's not clear at what point they do start aging. E.G. a tortoise that was presented to Captain Cook by the King of Fiji in the early 19th century is still alive in an Australian zoo.
- Turtle diversity: Turtles, despite their differences from all other amniotes, encompass a great deal of ecological variety. Although many are fresh-water aquatic, some are adapted to dry environments, and some are fully marine. Some are adapted for rapid swimming, some for a more leisurely mode.
- Phylogenetically, Testudines are pretty simple:
- Proganochelys: The first and most primitive turtle from the Late Triassic of Europe. Proganochelys could not retract its legs, head, or tail into its shell.
- Cryptodira: (hidden neck) The monophyletic group containing all turtles that pull their heads straight into their shells. (This includes most of the turtles you know.) Fossil record starts in Early Jurassic
- Pleurodira: (side-neck) The so-called side necked turtles, that fold their heads sideways against their bodies. These are found, today, only in the southern continents. Fossil record starts in Early Jurassic
VI. Long branch attraction: This leads us to a big theoretical issue in phylogenetic analysis.
- Chronology of hypotheses:
- During the late 1980s, Turtles were though to be related to t he captorhinids, a groups of small Permian reptiles close to, but not quite in Diapsida.
- In 1991, Reisz and Laurin indicated a possible close relationship between turtles and procolophonoids.
- In 1993, Michael Lee published your reading assignment, in which he proposed Pareiasaurs as a sister taxon. [In fact, according to later work by Lee, turtles may be a kind of pareiasaur.]
- Weirdest of all, in 1995, Olivier Rieppel performed a cladistic analysis that placed them inside Sauria, as members of Euryapsida (later) a group of marine reptiles.
- Finally, a 1997 molecular analysis makes them sister taxa of archosaurs. (Although I am told that this result changes radically depending on which turtle is included int he analysis.)
- Current Status: As things currently stand, most people have abandoned the captorhinid idea, but beyond this, no consensus exists.
The fossil record of turtles is partly to blame. In Synapsida, there was a very well documented gradual transition from primitive, to highly derived, mammal-like types. With turtles, no such transition is known. Proganochelys is primitive in some ways, but is unmistakably a turtle. We do not yet know any animal that is really intermediate between turtles and any other reptile group.
- Question to consider:
- What is the fundamental source of our difficulty (A: absence of enough intermediate states to allow phylogenies to be reconstructed reliably.
- Why so many different hypotheses? - Turtles are very derived. Inevitably, they have convergently evolved derived characters with other groups. Which hypothesis we trust depends on which characters we value.
- Examples of short and long branches:
- First, imagine a nice polite tree, in which lineages bifurcate at regular intervals. Now think of a character changing states on that tree, flipping back and forth between a 0 and 1 state. Such a phylogeny should be easy to reconstruct using PAUP, even despite the character reversals, because each change, be it from 0 to 1 or 1 to 0 would diagnose a node on the tree. This would be especially true, if there were many such characters.
- Now imagine a tree with relatively few branches that bifurcate early on then follow independent, non-bifurcating courses of evolution. Again, imagine a character flipping back and forth between two states. This time, when we attempt to reconstruct the phylogeny, we are in trouble. The character state changes on our long lonely branches do not diagnose new groups. Instead, they simply conceal the lineage's evolutionary history. When we perform an analyses of these characters, we are analyzing noise more than signal. As a result, we are likely to be positively misled byt he analysis because PAUP might construe random character changes on these long branches as synapomorphies. This is the long branch attraction problem.
- There are some hypothetical tree shapes in which the more characters you use, the more likely you are to be misled. This region of "tree-space" called the Felsenstein zone, after its discoverer, Joel Felsenstein.
- Conditions under which long branch attraction is a danger.
- Very rapidly evolving characters. When characters change states quickly in comparison to the rate at which lineages bifurcate, the danger exists. Some of the more improbable results of analyses of mammalian evolution using rapidly evolving mitochondrial DNA may be good examples.
- Very old branches with poor fossil record. Reliance on living taxa can often force us to confront long branches. This points out the real utility of fossils in phylogenetic analysis. Sure they are incomplete and, at best, sample only the anatomy of hard parts of the body, but they are real information from earlier stages of evolution that serve to break-up long branches.