The radiation of deep sea octopuses

By PZ Myers

Last week's [Friday Cephalopod](http://scienceblogs.com/pharyngula/2008/11/friday_cephalopod_antarctic_cu.php) actually has an interesting story behind it. It was taken from a paper that describes the evolutionary radiation of deep-sea cephalopods.

First, a little background in geological history. Antarctica is a special case, in which a major shift in its climate occurred in the last 50 million years. If you look at a map, you'll notice that Antarctica comes very close to the southern tip of South America; 50 million years ago, they were fully connected, and they only separated relatively recently due to continental drift.

antarctic.jpeg

When they were connected, South America acted as a barrier to ocean currents, shunting warmer water south to moderate Antarctica's temperature. The Antarctic waters at that time were a cool but pleasant 20°C. The two continents split apart about 34 million years ago, allowing rings of circumferential currents to surround Antarctica, isolating it from the warmer waters of the north and plunging it into a deep freeze; within a few tens of millions of years, the water temperatures dropped to about -1°C, the current temperature. It had almost certainly reached close to these frigid temperatures about 15 million years ago, when there was a strong expansion of the Antarctic ice sheet and the development of cold, deep currents emanting from the waters around the continent.

This kind of change in the environment imposes new stresses on the organisms living in it; there were also radical changes in the fauna of the Antarctic ocean concurrent with these temperature shifts. Sean Carroll describes these effects in his book, _The Making of the Fittest: DNA and the Ultimate Forensic Record of Evolution_([amzn](http://amazon.com/exec/obidos/ASIN/0393330516/pharyngula-20)/[b&n](http://service.bfast.com/bfast/click?bfmid=2181&sourceid=41505966&bfpid=0393330516&bfmtype=book)/[abe](http://www.dpbolvw.net/click-1772498-9836638?url=http%3A%2F%2Fwww.abebooks.com%2Fservlet%2FSearchResults%3Fisbn=0393330516&cm_ven=CJ&cm_cat=1616003&cm_pla=1772498&cm_ite=Abebooks-Book+Redirection+Allowed)/[pwll](http://www.powells.com/cgi-bin/partner?partner_id=30010&cgi=product&isbn=0393330516)) (which I recommend highly), in which he discusses the evolution of notothenioid fish, the icefishes. These animals survived the gradual cooling by the evolution of antifreeze proteins, modifications to their cytoskeleton that made them more stable in the cold, and reduction of, and in some cases complete loss of, red blood cells to reduce blood viscosity. It's a very cool story in which geological events are neatly correlated with molecular changes, as Carroll diagrammed below.

timeline.jpeg

Not just teleost fish had to adapt, obviously — the invertebrates of the region faced the same stresses. The current work did not address the physiology of Antarctic cephalopods (I hope someone does, though!), but looked instead at the relationships between Antarctic octopus species and deep sea octopus species. They noticed a similar interesting correlation: the lineages diverged approximately 33 million years ago, and there was a subsequent radiation of new forms into deep ocean waters about 15 million years ago. The cladogram below illustrates the pattern — the cephalopods endemic to the Antarctic are in blue, while deep sea octopuses, which are found far, far north of the Antarctic, are in red. They're related!

cladogram.jpeg
(Click for larger image) Phylogenetic relationships of Southern Ocean endemic and deep-sea octopuses. Bayesian phylogenetic tree based on the results of the relaxed phylogenetic analysis utilizing the seven genes: rhodopsin, pax-6, octopine dehydrogenase (ODH), 12S rDNA, 16S rDNA, cytochrome oxidase subunit I (COI) and cytochrome oxidase subunit III (COIII) of 12 Antarctic octopus species, seven deep-sea octopus species and 15 outgroup taxa. The topology is that from the posterior sample which has the maximum sum of posterior probabilities on its internal nodes. Each node in the tree is labelled with its posterior probability, * indicates a posterior probability of 1.0. The divergence times correspond to the mean posterior estimate of their age in millions of years. The genera Adelieledone (dark blue), Pareledone (blue), and Megaleledone (light blue) are endemic to Antarctic waters. The deep-sea genera, Graneledone (red), Velodona (yellow), and Thaumeledone (orange) are a monophyletic group and are nested within the Antarctic clade. The deep-sea clade was estimated to have originated around 33 millions years ago (Ma; 95% HPD interval 5-64 Ma). The three deep-sea genera were estimated to have diverged from one another around 15 Ma (95% HPD interval 1-36 Ma). Depth ranges were taken from the literature as follows except for P. turqueti and A. polymorpha (Allcock, unpublished data): A. piatkowski (Allcock et al., 2003a), Pareledone spp. except P. turqueti (Allcock, 2005), M. setebos (Allcock et al., 2003b), G. antarctica (Voss, 1988; Vecchione et al., 2005), G. verrucosa (Allcock et al., 2003c), G. boreopacifica and V. togata (Voss, 1988), T. peninsulae (Allcock et al., 2004; Strugnell et al., 2008), other Thaumeledone spp. (Allcock et al., 2004).

The map below gives the geographic perspective — these species are dispersed over a large part of the world's oceans, from an origin in the Antarctic.

distrib.jpeg

Distribution of deep-sea octopus species showing the southern focus of their distribution. Includes all species of Graneledone (red), Thaumeledone (orange), and Velodona (yellow) according to most recent taxonomic revisions of each group. Blue line is schematic pathway of the Antarctic Bottom Water flows of the thermohaline circulation from Rahmstorf, 2006 (18) re-projected using the Lambert Azimuthal Equal Area projection.

It's developing into a powerful evolutionary story. Geographic isolation and environmental change lead to adaptation of local species, and the adaptations to these special conditions, cold and darkness, open up new niches in the deep sea for these animals. Their distribution is further abetted by currents that formed 15 million years ago, when cold Antarctic surface waters sank and flowed north in the deep ocean, carrying pre-adapted cephalopods with it.

Strugnell, JM, Rogers AD, Prodo PA, Collins MA, Allcock AL (2008) The thermohaline expressway: the Southern Ocean as a centre of origin for deep-sea octopuses. Cladistics 24:1-8