Diving Into the Past

How long can you hold your breath underwater? I’ll wager it wouldn’t be for much longer than a minute or two at most. The world record for a human is an astonishing 22.3 minutes set by Tom Sietas in June 2012 (link here). He did accomplish this with the aid of breathing pure oxygen for 30 minutes beforehand. The record without any aid is still an amazing 11.5 minutes. These extreme examples aside, the majority of the world’s population would struggle to achieve anything over two minutes. However, not all our mammalian cousins are as inept at staying submerged as us humans, especially those lineages that have returned the sea, such as the cetaceans (whales and dolphins), pinnipeds (seals) and sirenians (dugongs and manatees). These animals have evolved to be able stay underwater for much longer periods of time, with the longest dives undertaken by the northern elephant seal and the sperm whale, both of whom can dive for over an hour on a single breath! Marine mammals have evolved a whole suite of anatomical and physiological adaptations to enable themselves to undertake these long dives but key to their underwater exertions is the increased ability to store oxygen in their muscle tissues.

A model of a myoglobin molecule from a sperm whale. Image from en.wikipedia.org
A model of a myoglobin molecule from a sperm whale. Image from en.wikipedia.org

The protein molecule that allows mammals to store oxygen in their muscle tissues is known as myoglobin (in your blood oxygen is carried by haemoglobin). You can tell when this respiratory pigment is present in tissue as it gives it its red colour and, as any of you who have dissected a whale, dolphin or some other marine mammal will know, the elevated concentrations in their tissues cause their tissues to be very dark, even almost black in colour. Myoglobin is one of the best known and studied proteins but researchers were still unsure how marine mammals could use myoglobin in such high concentrations as it tends to clump and stick together when present in large amounts, therefore obviously making it difficult for it to be able to store oxygen in the body’s tissues.

A new paper published in the journal Science just over a week ago claims to have unravelled how marine mammals can take advantage of the elevated myoglobin concentrations and not get their tissues clogged up by the protein (Mirceta et al, 2013). What the researchers found was that mammalian divers have higher net surface charges on their myoglobin molecules, namely higher positive charges. What this does is cause the myoglobin molecules to stay apart from each other as (remember your high school physics) like charges repel, allowing there to be lots more myoglobin without it clumping together.

Graph showing how as the net surface charge (Zmb) increases, so does the concentration of myoglobin (Mbmax). Image from Mirceta et al. 2013.
Graph showing how as the net surface charge (Zmb) increases, so does the concentration of myoglobin (Mbmax). Image from Mirceta et al. 2013.

But what has this got to do with fossils I hear you ask? This is meant to be a palaeontology blog, not a physiology one! Well this is where an already interesting paper becomes even better. As the relationship between this increased net surface charge of the myoglobin molecules and the increased levels of myoglobin was statistically very robust, this allowed the researchers to use a process called ancestral sequence reconstruction to estimate what the myoglobin sequences of extinct mammals were and therefore estimate their diving capabilities!

Cool figure showing the evolutionary reconstruction of myoglobin net surface charge in terrestrial and aquatic mammals. Image from Mirceta et al. 2013.
Cool figure showing the evolutionary reconstruction of myoglobin net surface charge in terrestrial and aquatic mammals. Image from Mirceta et al. 2013.

There were several interesting results obtained from the ancestral sequence reconstruction, which was conducted for a 130 species phylogeny. It suggests that some extant terrestrial mammals actually may have had an amphibious ancestry. This may not sound immediately intriguing but when you consider that the groups they imply are taxa such as echidnas and moles, both of whom are very well adapted to a fossorial (digging/underground) lifestyle then it really does become more noteworthy. Interestingly, close relatives or even members of both groups (e.g. the platypus and the star nosed mole) still have an amphibious lifestyle. Another group which was found to have an amphibious ancestor was the Paenungulates. This large group contains terrestrial animals such as elephants and hyraxes as well as aquatic taxa such as dugongs, manatees, and the extinct desmostylians. Aquatic ancestry has long been debated for elephants and their kin (known as the Proboscidea) and this study provides evidence for a fossil species of proboscidean possessing a higher net surface charge of its myoglobin, with the modern levels representing a secondary reduction in net surface charge.  The authors themselves note that an aquatic ancestry for the hyraxes may seem surprising when current diversity is considered, but there are much larger fossil species for which a semiaquatic lifestyle has been proposed in the past. Another interesting point is that if the common ancestor of the Paenungulates was indeed aquatic, it would represent the earliest placental mammal radiation into the aquatic realm. At an estimated 64 million years ago it would predate the cetaceans and the pinnipeds reinvasion of the water.

Figure showing the evolution of myoglobin net surface charge and aquatic habits in Afrotheria. Note how the fossil proboscidean Moeritherium was more aquatic than modern taxa. Image from Mirceta et al. 2013.
Figure showing the evolution of myoglobin net surface charge and aquatic habits in Afrotheria. Note how the fossil proboscidean Moeritherium was more aquatic than modern taxa. Image from Mirceta et al. 2013.

Furthermore, by using the relationship between maximum dive time, muscle myoglobin concentration and body mass in extant (living) species, they also estimated maximum dive time in extinct species too (using estimates of body mass for the extinct species). This type of ecological information has been nothing more than an educated guess based on morphology and internal bone structure until now, where Mirceta et al. have constructed a robust model to estimate the dive times of extinct taxa. From their model the team have estimated that one of the earliest known cetaceans, the early Eocene Pakicetus could only hold its breath for 1.6 minutes, whereas by the late Eocene, cetaceans had evolved to the point where Basilosaurus was capable of staying submerged for 17.4 minutes, a figure comparable to modern dolphins. In pinnipeds, the earliest known taxon Enaliarctos has an estimated maximum dive time of 4.7 minutes, which is poor compared to modern seals, perhaps reflecting the fact that it hunted in shallower waters than its modern counterparts? In the proboscideans (the group containing elephants, mammoths, mastodons etc.), the secondary change back to a terrestrial lifestyle (already mentioned above) is reflected in the result that a fossil proboscidean (Moeritherium) had an estimated dive time of 10 minutes, compared to 2.5 minutes in the modern Asian elephant.

Graphs showing diving capacity in ancestral whales, seals, and sea cows. Image from Mirceta et al. 2013.
Graphs showing diving capacity in ancestral whales, seals, and sea cows. Image from Mirceta et al. 2013.

This is a really fascinating paper and the best thing about it is that it gives researchers a whole new raft of hypotheses to go away and test. This shows what can be done when a multidisciplinary approach is used in the right way, integrating molecular technologies and fossil data to produce insights that would have been thought impossible previously, giving scientists a new way to think about their fields. Science, you’ve done it again.

References

Mirceta S, Signore AV, Burns JM, Cossins AR, Campbell KL, Berenbrink M (2013) Evolution of Mammalian Diving Capacity Traced by Myoglobin Net Surface Charge. Science 340: 1234192.