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

Physics versus biology

When I was in high school, my physics teacher drew a massive rectangle that took up almost the entire black board and proclaimed, "this is physics". He then drew a little rectangle inside the first one and proclaimed, "this is biology". The he made a tiny little smudge of chalk on one of the sides of the 'biology' rectangle and said, "this is chemistry, so you all should study physics because all the other major division of science are just sub-disciplines of physics".

Amusing as his performance was, there are many aspects of biology that cannot be directly or indirectly inferred from our understanding of physics. Notably, we would have never formulated the theory of evolution, which underpins our modern understanding of biology, if we had to rely on progress in physics alone. Clearly though, physics is important in shaping the evolution of particular traits. I've written many times about physics in biology, such as swimming in sharks (here), flight in albatross (here), the hammer strike of mantis shrimp (here) and the visual capability of giant and colossal squid (here and revisited here).

Almost all organisms that detect and use light do so in the same part of the spectrum, which is pretty much the same part of the spectrum we see in. Although many use slightly shorter wavelengths in the ultraviolet or slighter longer wavelengths in the infrared, no organisms that we know of use the huge parts of the spectrum in the radio, x-ray and gamma ray wavelengths. I've wondered why this is before, but Mathew Cobb wondered it out loud and got some interesting answers.

Everyone loves bacon

Researchers at the VENUS Observatory put a pig carcass in 300 meters of water and watched to see what came to eat it. Mostly amphipod crustaceans, it would seem.

Results vary only slightly when the carcass is not in a cage. The wounds that appear early in the video are caused by sharks, I'm pretty sure.

Hermit crab migration

On Tuesday I wrote about a crustacean with an unusual larval form. The larvae occur in mid-water while the adults occur in the deep sea. Habitat shifts associated with changes in life history stage are not uncommon and some of them are even more dramatic than changing depth. Take the hermit crabs in the Virgin Islands. The adults are terrestrial, but the larvae develop in the sea. The adults must migrate to the waters edge in order to reproduce and release their eggs into the water.

Hermit Crab Migration from Steve Simonsen on Vimeo.

Hermit crabs are not true crabs. True crabs are in the crustacean infraorder Brachyura, while hermit crabs are in the infraorder Anomura. There are Brachyurans that perform similar mass migrations to release their eggs into the sea. One of the best known is the migration of the Christmas Island crab.

If the eggs and larvae survive out in the ocean, tiny juveniles climb back onto land and migrate into the forests where they grow into adults. In most years, only a very small number will make it back to land. In some rare years, the numbers that arrive on the shore are mind-boggling.

An unusual crustacean meets its parents

Many animals living in the ocean have complex life histories where the young look nothing like the adults and often occupy different habitats. Frogs, with their early tadpole stage, are classic examples of animals with complex life histories. But, tadpoles look far more like frogs than the larvae of other animals resemble their adult forms. Different species of distantly related crustacean larvae, for instance, can look far more like each other than they resemble the adults of their own species.

The nuaplius larvae stage (left) of a cylopoid copepod (top) and penaeid shrimp (bottom) and their adult forms (right). These distantly related crustaceans appear similar as larvae, but not as adults (images Wikipedia)

Because larvae look so different from the adult form, identifying the species that larvae belong to can be tricky. Often it requires the larvae to be carefully reared in the laboratory to see what they eventually turn into, but this isn't always possible. In some cases, it is possible to place larvae within a species using genetic techniques, but this requires a DNA sequence from the adult to compare to.

One type of crustacean larva that has been difficult to assign to an adult form are the Cerataspids. There are three known species that have been placed in two genera, Cerataspis monstrosa, C. petiti and Cerataspides longiremus. Like many unusual crustacean larvae, the first to be discovered (C. monstrosa in 1828) was thought to be an adult of the crustacean order Leptostraca. However, it later became apparent that they were probably larvae of shrimp within the Penaeoid superfamily, possibly from the family Aristeidae.

The crustacean larva Cerataspis monstrosa (image from Bracken-Grissom et al. 2012)

Through a combination of skill and luck, Bracken-Grissom et al. were able to resolve the adult identity of C. monstrosa. The luck involved getting their hands on a specimen of the larva that was suitable for DNA analysis. Almost all we know about C. monstrosa comes from examining specimens in the gut contents of its predators, like skipjack tuna. But, Bracken-Grissom et al. unexpectedly obtained a single specimen from a trawl at a depth of 420 meters in the Gulf of Mexico.

Bracken-Grissom et al. collected DNA sequence data from the specimen and compared it to sequences of crustaceans available from a database of genetic sequences. Because C. monstrosa had been liked with Penaeoid shrimp in the family Aristeidae, they concentrated their analysis within those taxonomic groups. And they hit pay dirt. The DNA from the C. monstrosa specimen was a near perfect match with a deep-sea Aristeid shrimp Plesiopenaeus armatus.

The Aristeid shrimp Plesiopenaeus armatus (image from Bracken-Grissom et al. 2012)

Plesiopenaeus armatus has a similar geographic distribution to C. monstrosa, but it is known from deeper water. The contrast between the larval habitat and  adult habitat is not unusual for organisms with complex life histories. Indeed, many complex life histories involve much more dramatic habitat shifts. However, the transition from mid-water pelagic larvae to abyssal adults is not known in many species.

The findings of Bracken-Grissom et al. have implications for the other species of Cerataspis larvae that haven't been linked to their adult form. They suggest that C. petiti is the larva of the only other known species in the genus Plesiopenaeus, P. coruscans. Further they suggest that Cerataspides longiremus is the laval stage of a closely related Aristeid shrimp, possibly an unidentified representative of the same genus.

Bracken-Grissom HD, Felder DL, Vollmer NL, Martin JW, & Crandall KA (2012). Phylogenetics links monster larva to deep-sea shrimp Ecology and Evolution DOI: 10.1002/ece3.347

High impact science

The exoskeletons of arthropods allow them to do many seemingly preternatural things. Storing energy to generate the fastest limb movements in the animal kingdom is one of those things. Stomatopods, or mantis shrimp, aren't the fastest, but the hero of this story (Odontodactylus scyllarus) can accelerate its killing arms incredibly fast (65 - 104 km s^-2) reaching top speeds of 23 meters per second. To my knowledge, that's the second fastest limb movement ever recorded. And it's performed in water, which strongly limits speed relative to air.

The stomatopod Odontodactylus scyllarus, or peacock mantis shrimp (photo Wikipedia)

Stomatopods are coarsely divided into two groups based on the shape of their killing arms. Some stomatopods have arms that look similar to those of praying mantises, which is where their common name is derived. These stomatopods are called "spearers", as they use their arms to impale soft-bodied prey. The other group, which use club-like arms to break open the shells of other crustaceans and mollusks, are called "smashers". But, there is a great diversity in the form and function of stomatopod arms. The largest stomatopods tend to be spearers, but the fastest are smashers.

A sample of the diverse shapes of stomatopod killing arms (photo Thomas Claverie)

Our speedy pal, O. scyllarus, is a relatively large smasher, growing to 18 centimeters. Although water does hamper the speed of its strike, it also provides an interesting advantage. The fast movement of the club-like killing arm causes a cavitation bubble to form between the club and the point of impact. Cavitation bubbles form in areas where water pressure drops so low it forces a phase change from liquid to vapour. The higher pressure in the surrounding water then causes the vapour bubble to collapse rapidly, releasing a shock wave of sound and a burst of light. The collapse of the cavitation bubble is so violent that it can impart a force as great as the club strike on the prey item.

 

The stomatopod O. scyllarus in action

The double strike of the club and cavitation bubble causes an impressive amount of damage to the hard-shelled prey of O. scyllarus. But, the impact of the strike and cavitation bubble also cause damage to the club itself. The only time this damage can be repaired is when the stomatopod moults. Although O. scyllarus does moult relatively frequently, its clubs are still resilient enough to deliver thousands of blows between moults.

The resilience of the club's hitting surface is due to a complex, three-region architecture that allows small cracks to form, but prevents them becoming large enough to be a problem. The outer 'impact region', which forms the hitting surface, contains a highly crystalised form of the mineral hydroxyapatite. The inner 'periodic region' also contains hydroxyapatite, but here it occurs in the amorphous mineral phase and is interspersed with the carbohydrate chitin, which is arranged in helical stacks. The 'striated region', which forms the back and sides of the club, is made of chitin arranged in circumfrential bands.

Cross sections of an O. scyllarus club, illustrating the three-region architecture. The crystalised hydroxyapatite impact region, the amorphous hydroxyapatite and chitin periodic region and the chintinous striated region. The lower panel shows the distribution withing the club; blue for the impact region, red and yellow for the periodic region and green for the striated. The orange indicates another segment of the killing arm that sits behind the club and acts as the 'handle' (image modified from Weaver et al. 2012).

The periodic region is the 'shock-absorber' of the system and the majority of cracks that form in the club occur in this region. The cracks that form are forced to twist inwards by the helically arranged chitin and are largely prevented from spreading between layers or into the impact region. The striated region of chitin reduces the deformation of the club during strikes and helps to keep the cracks contained within the periodic region. This unique architecture allows the club to survive the damaging forces of many high speed strikes on hard-shelled prey.

If you would like to hear more about the fast strike of O. scyllarus, including high speed footage of the cavitation bubble and images of damage to the club, I recommend you check out Shelia Patek's TED talk.

References:

Patek, S., Korff, W., & Caldwell, R. (2004). Biomechanics: Deadly strike mechanism of a mantis shrimp Nature, 428 (6985), 819-820 DOI: 10.1038/428819a

Weaver, J., Milliron, G., Miserez, A., Evans-Lutterodt, K., Herrera, S., Gallana, I., Mershon, W., Swanson, B., Zavattieri, P., DiMasi, E., & Kisailus, D. (2012). The Stomatopod Dactyl Club: A Formidable Damage-Tolerant Biological Hammer Science, 336 (6086), 1275-1280 DOI: 10.1126/science.1218764