Living fossils are evolving

Charles Darwin coined the term living fossil in On the Origin of Species. He didn’t use it the same way that it has come to be used. He suggested that living fossils are modern species that can be used to link to groups in the same way that fossils can. One of the examples he gave was the platypus, which lactates and lays eggs, which is evidence that mammals and reptiles share a common ancestor. I don't think he meant it to mean an unchanged relict, as some people interpret his words.

Today, a living fossil is a species that retains many features of their fossil ancestor so that it is recognisably closely related. There are some stunning examples of this, such as orb-weaving spiders. In 2011 a 165 million year old spider fossil was described by Seldon et al., which shared so many features with modern Nephila spiders that it was placed within the same genus. Interestingly, I have never heard of web building spiders being referred to as living fossils despite there being amazing conservation of traits in many groups.

The orb-weaving spiders Nephila clavipes (left) and N. jurassica (right) are separated by 165 million years, but placed within the same genus (image of N. clavipes from Wikipedia and N. jurassica from Seldon et al. 2011).

Unfortunately, living fossil has become synonymous with a species, or group of species, displaying no evolutionary change or very slow change. This is completely wrong. Although the conservation of morphology in Nephila is remarkable, there are more than 150 known species in the genus. Clearly there has been evolutionary diversification within the group. Indeed, whenever living fossils are examined in more than superficial detail it becomes difficult to see them as organisms that evolution forgot.

Horseshoe crabs are one of the most iconic living fossils. There are four living species in three genera. They are placed within the subphylum chelicerata, which makes them more closely related to spiders and scorpions than they are to true crabs, which are placed within the subphylum crustacea. Although there are fewer species of horseshoe crabs than Nephila, that fact that there are four species that are all different from fossil species is a strong indication that evolution hasn't stopped for them.

The Atlantic horseshoe crab, Limulus polyphemus, mating (photo Wikipedia)

The general shape of modern horseshoe crabs is strikingly similar to the fossils that date from about 450 million years ago. Close examination, though, shows that parts of their shape, their legs in particular, have changed over time. Briggs et al. 2012 looked at a fossil horseshoe crab from 425 million years ago, which is relatively early in their evolution. They found that modern horseshoe crabs are missing an entire set of limbs that were present in their ancestors.

All modern chelicerates, including living horseshoe crabs, have unbranched limbs; each limb is a single series of segments. Most crustaceans have limbs that branch at the base into two series of segments. Branched limbs, like those in crustaceans, are the ancestral condition and unbranched limbs are thought to have evolved several times among the arthropods. Indeed, Briggs et al. found that the fossil horseshoe crab had branched limbs, which have been lost in their descendents. 

Like horseshoe crabs, tadpole shrimp have a broad semi-circular carapace protecting their heads and are considered living fossils. There are 11 recognised species in two genera, Lepidurus and Triops. The two genera probably diverged about 180 million years ago, but there are fossil tadpole shrimp dating from about 250 million years ago. That's not as long as the really iconic living fossils, like horseshoe crabs and the coelacanths, but it is still an impressive amount of time to retain enough features to be easily recognised as related.

The tadpole shrimp, Lepidurus apus (photo Wikipedia)

The problem with relying on features that preserve in the fossil record is that it underestimates the actual amount of evolutionary change because generally only hard parts are preserved. A recent study of tadpole shrimp highlights this point. Mathers et al. 2013 used genetic analyses to construct the evolutionary relationships among the 11 species of tadpole shrimp. They found that there are actually 38 species and that these species arose relatively recently. This shows that rather than evolutionary stasis, there is likely to be high species turnover in the group.

There are many reasons why some features may be conserved over long periods of time. None of these have to do with natural selection taking a break. In fact, if natural selection did cease we should expect to see features wander under random genetic drift, as has been hypothesised for eyes in cave dwelling animals. Conserved features are much more likely to be the result of developmental constraints or stabilising selection.

References:

Briggs, D., Siveter, D., Siveter, D., Sutton, M., Garwood, R., & Legg, D. (2012). Silurian horseshoe crab illuminates the evolution of arthropod limbs Proceedings of the National Academy of Sciences, 109 (39), 15702-15705 DOI: 10.1073/pnas.1205875109 

Mathers, T., Hammond, R., Jenner, R., Hänfling, B., & Gómez, A. (2013). Multiple global radiations in tadpole shrimps challenge the concept of ‘living fossils’ PeerJ, 1 DOI: 10.7717/peerj.62

Selden, P., Shih, C., & Ren, D. (2011). A golden orb-weaver spider (Araneae: Nephilidae: Nephila) from the Middle Jurassic of China Biology Letters, 7 (5), 775-778 DOI: 10.1098/rsbl.2011.0228

Curiosities of evolution - Part I: Birds and viviparity

Evolution by natural selection is often incorrectly thought of as an unbounded path to novelty. I was reminded, when writing about coelacanths and manta rays, that there are some traits that are curiously absent from some lineages. In particular, the birth of live offspring (viviparity) has independently evolved many times in a diverse range of taxa, but not in birds or, probably, any other dinosaur (birds are theropod dinosaurs). Many adaptive explanations have been proposed to explain why this might be the case.

There are many ways that live birth can occur and many ways that the mother can provide nourishment to her offspring. The extant coelacanths, for instance, are what's known as 'oviviviparous', because females retain their eggs within their body until their offspring hatch, at which point the mother gives birth. Manta rays too, are oviviviparous, but mothers supply extensive additional nutrition after their offspring hatch.

In oviviviparous animals, the yolk allocated to the egg can be the only nourishment that offspring receive. But, there is a continuum from total reliance on the yolk, through various amounts of additional nutrition supplied by the mother (matrotrophy), to examples where all nutrition is supplied by the mother without yolk. Matrotrophy can be achieved with or without a placenta, and sometimes in alien ways, such as the cannibalism of siblings and unfertilised eggs within the uterus. Animals that are considered 'truly' viviparous are often only those where matrotrophy is complete.

After the ray-finned fishes, birds are the most species-rich lineage of vertebrates, yet not one species produces live young. The available evidence suggests that all dinosaurs were also egg laying. This is curious because all other major vertebrate groups, with the exception of the agnatha, have multiple examples (at least 120) of the independent evolution of live birth. And, unlike the agnatha, birds have several of the traits thought to be required for viviparity, like internal fertilisation.

Many hypotheses have been proposed to explain the lack of viviparity among birds; flight and the hard-shelled egg are the two explanations that seem to best fit the data. Pterosaurs, like birds, flew and seem to have all been egg laying. And bird's eggs are relatively impermeable to gas exchange when compared to those lineages of reptiles that have evolved viviparity. Indeed, turtles and crocodilians have similar hard-shelled eggs and have also not evolved viviparity.

However, these two hypotheses aren't completely satisfying. The 'flight-as-a-constraint' hypothesis is contradicted by live birth in bats and doesn't explain why none of the many flightless birds and dinosaurs evolved viviparity. The 'egg-as-a-constraint' hypothesis hinges on oxygen being a limitation and the assumption that the eggshell cannot be eliminated through evolution. But birds lay their eggs well before oxygen limitation would become a problem for embryos. And the evolution of viviparity in other lineages seems to begin with a lengthening of the period that eggs are retained before they are laid, only later does the eggshell thin to increase oxygen availability.

Some authors have suggested that viviparity has not evolved because directional selection for egg retention must be absent in birds, or that there is selection against it. The argument behind this hypothesis is that many of the advantages that viviparity may confer are solved by other means in birds and viviparity may have negative effects on mothers. For instance, retaining eggs internally may reduce the predation risk for offspring by decreasing the amount of time they're highly vulnerable to predators. But conversely, it may increase the risk of predation for mothers because they must carry an extra weight that could reduce their ability to escape.

Here too, counter examples can be found. For instance, there may be a selective advantage of egg retention in some species where eggs are a small fraction of maternal body mass and external incubation is costly. Many seabirds travel long distances between nesting sites and feeding grounds and they are also often large relative to the size of the egg. This suggests that carrying the extra weight of an egg is a minor cost and that there may be an energetic advantage to reducing the period of external incubation.

Other authors have suggested that the reason egg retention is short in birds is that their body temperature is too high for developing embryos. The resting temperature of birds is nearly universally 40 - 41 °C, while the optimal incubation temperatures are between 34  °C and 38 °C. Body temperature may, therefore, be a physiological constraint on egg retention in birds. But, correlation is not causation. Optimal incubation temperatures may have evolved because they're the temperatures that eggs are normally incubated at, not because they're the maximum temperatures that embryos can tolerate.

To me, the body temperature hypothesis probably carries the most weight as an adaptive explanation, but it remains untested. And, although the lack of viviparity in birds cries out for an adaptive explanation, we should not assume that the presence of absence of particular traits is the result of adaptive mechanisms. Nevertheless, the lack of viviparity in birds and other dinosaurs is an interesting and unresolved evolutionary question.

References:

Blackburn, D. G., & Evans, H. E. (1986). Why are there no viviparous birds? The American Naturalist, 128 (2), 165-190 DOI: 10.1086/284552 

Anderson, D. J., Stoyan, N. C., & Ricklefs, R. E. (1987). Why are there no viviparous birds? A comment. The American Naturalist, 130 (6), 941-947 DOI: 10.1086/284757

The evolution of living fossils

The term 'living fossil' is a problematic one because its meaning is so frequently misunderstood. The greatest misunderstanding is that a living fossil species has not evolved for tens or even hundreds of millions of years (e.g. anatomically modern coelacanths are know from 409 mya). But, this is completely and utterly wrong. Living fossils are species that are related to, and superficially resemble, other species from the fossil record. But, they can be morphologically distinguished from the fossil species and have almost certainly evolved in ways that don't preserve in stone (e.g. behaviourally, physiologically and immunologically).

Three species of coelacanth. The top two are the fossil species Coelacanthus and Macropoma, while the bottom is the extant specie Latimeria. Note that they are all similar, but easily distinguished.

So, it's a little disappointing when a usually very good science news website perpetuates this misunderstanding by starting a popular science article like this: 

The morphology of coelacanths has not fundamentally changed since the Devonian age, that is, for about 400 million years. Nevertheless, these animals known as living fossils are able to genetically adapt to their environment.

There is nothing at all surprising about populations of living fossils containing enough genetic diversity to adapt to the environment. And there is simply no good reason to assume that their genetic diversity will be any different to any other extant species. 

The paper itself does not make this mistake. The interesting thing about studying the genetic diversity of coelacanths is not because they are living fossils, but because they are considered rare and endangered. A good understanding of genetic diversity within populations and an understanding of gene flow among populations can be very informative for the development of conservation management strategies. And this is the aim of the paper.

The authors obtained genetic material from 71 adult coelacanths from 6 locations across the entire known range of Latimeria chalumnae, the East African coelacanth (L. menadoensis is a second species found off Indonesia). The genetic diversity among the coelacanths was low, as would be expected from their small population sizes. The largest population of 300 - 400 individuals occurs off the Comoros Islands and all other populations appear to derive from it. The greatest genetic diversity, however, was found in populations from Tanzania.

The sites that genetic samples were collected from. The size of the circles indicates the sample size (key at bottom) and the colours indicate the genetic types found in a population (taken from the paper).

The genetic differentiation between the Comoros population and populations in other locations shows that adaptation is still occurring, but that there is unlikely to be much gene flow among populations. Interestingly, and completely unexpectedly, there appears to be two genetically distinct populations occurring at the same locations within the Comoros Islands. It's unclear what factors are driving the differentiation in the two Comoran subpopulations.

The genetic differentiation between the populations along the African coast isn't strong. This suggests that either the populations diverged relatively recently, or that they're evolving slowly. Curiously, the authors argue that their results confirm that the coelacanths are evolving slowly. But, their data can't separate these two hypotheses. Other studies show that the genes which control morphology are evolving slowly (surprise!), but other gene regions are within the evolutionary rates for vertebrates and consistent with rates in sharks, which have similar life histories. It seems more likely, therefore, that the populations have diverged relatively recently, suggesting that populations could be being recolonised from the Comoros Islands after local extinctions. 

So, coelacanths, like other living fossils, are evolving just fine. Their populations off East Africa look to have reasonably good genetic diversity for their population numbers. But, populations will probably need to be managed separately because there is little gene flow among them.

Reference:

Lampert KP, Fricke H, Hissmann K, Schauer J, Blassmann K, Ngatunga BP, & Schartl M (2012). Population divergence in East African coelacanths. Current biology, 22 (11) DOI: 10.1016/j.cub.2012.04.053

Older fourlegs

China seems to have had the lion's share of the cool fossils unearthed in the last 10 years or so. A new   paper¹ on a coelacanth fossil from south China is another example of their phenomenal treasure trove of fossils. It pushes back the origin of anatomically modern coelacanths by 17 million years to 409 million years ago. The previous oldest coelacanth was known from a jaw found in Australia. 

Coelacanths are interesting for many reasons, not least because they are more closely related to us than they are to other fish. The group was though to have gone extinct around the same time as the dinosaurs, 65 million years ago. But, in 1938 an extant representative was found in South Africa (although it had been known by the local fishermen for a while before that). A book about the discovery dubbed the fish 'old fourlegs'. There was more excitement in 1997, when a second extant species of coelacanth was found off Indonesia.

A preserved specimen of the extant coelacanth, Latimeria chalumnae, or old fourlegs.

The modern coelacanths look almost the same as their ancestors did a few hundred million years ago. So, much like the sharks, they represent 'living fossils'. To put their ancient history in a little perspective, about the same time as the anatomically modern coelacanth body plan emerged, our ancestors were probably taking their first steps on land². 


References:
1 Zhu, M., Yu, X., Lu, J., Qiao, T., Zhao, W., and Jia, L. (2012) Earliest known coelacanth skull extends the range of anatomically modern coelacanths to the Early Devonian. Nature Communications 3, doi: 10.1038/ncomms1764


2 Niedz´wiedzki, G., Szrek, P., Narkiewicz, K., Narkiewicz, M., and Ahlberg, P. E. (2010) Tetrapod trackways from the early Middle Devonian period of Poland. Nature 463, 43 - 48.