Unravelling the secret diversity of Psychropotes! A global sea cucumber mystery!

via the NOAA photo library http://www.photolib.noaa.gov/htmls/expl6751.htm

Today we look at one of the most bizarre deep-sea echinoderms (if not deep-sea ANIMALS) that I know of! the sea cucumber Psychropotes!!  I briefly discussed these in an earlier post on deep-sea sea cucumbers.. but have not had the pleasure of writing something up about them in detail..

Here's some video to give you an idea of what it looks like/how it moves, etc. (I would watch without sound to enjoy the zen of the animal)
               
IF the name doesn't sound familiar, the animal's distinctive appearance definitely stays glued in your head after you've seen one! Imagine a big blobby sea cucumber with what looks to be a HUGE LOBE sticking out of its hind end!


Note the image above contrasted to this diagram showing mouth (top) and anus end (with lobe-bottom).

The genus Psychropotes is derived from the Greek for Psychros which means "cold or frigid" and "potes" which honestly, I could not find a definitive translation for...   One root translated to "flight"? possibly alluding to the ability of this species to swim...And another colleague tells me it might mean "dweller". Ah well, one mystery at a time!!

Psychropotes includes 11 species which occur widely, all around the world in the Atlantic, Pacific, Indian and Southern (but not in the Arctic) oceans in the deep abyss of the world's oceans! That means roughly 2000 to 6000m. They are the deepest of the deep! Considered "classic" deep-sea inhabitants they were collected and described from the HMS Challenger's historic mission.

These can be pretty BIG animals!! as this image from a recent MBARI expedition demonstrates. (with deep-sea biologist Greg Rouse for scale!)

From MBARI https://twitter.com/sarahkeartes/status/593979334056022016

But there is ONE species in particular, P. longicauda (the species name "longi-" means long and "caudex" refers to 'trunk or stem" and alludes to the posterior lobe in the same way that caudal fin refers to the end of a fish) that is of interest.

Individuals all identified as this species, P. longicauda have been observed from oceans all around the world and varies rather widely in many ways. Sea cucumber species are identified based on tiny calcite bits called sclerites which seem to be highly variable.. with differences in sclerite shape varying between different regions.  But do all of these differences amount to different species?  Or variation within ONE species?? 

Here for example was one seen from the recent tropical Pacific Okeanos Explorer cruises. Note that the "lobe" is a different shape. Separate species? Damage? 

This turns out to be a pretty important question to deep-sea biologists. Can there be ONE species present at such a huge scale? Or are there species present that are CRYPTIC or hidden from us by body characteristics alone???

Note the one above with the shorter, forked "lobe" Is it the SAME species as the purple one shown earlier? Is this variation? (such as what we might see in humans who live in different parts of the world) Or are these separate species?

A NEW paper by Chrysoula Gubili at the University of South Hampton and other coauthors from Southampton, including Elizabeth Ross and Paul Tyler in Deep-Sea Research II  was just published a few months ago exploring the population geography of this globally occurring deep-sea species! 

Their study explored the widespread occurrence of this species based on 128 specimens of Psychropotes longicauda collected from THREE different oceans over a 34 year period, from 1977 to 2011!

This represented an INTERNATONAL team of experts from not only the University of Southampton in the United Kingdom but also the Shirshov Institute of Oceanology in Russia, the American Monterey Bay Aquarium Research Institute (MBARI), Scripps Institute of Oceanography and many, others!! 

They sampled tissue for two genetic markers (COI and 16S for those who need to know) across all the sampled individuals in order to compare populations from all around the world. 

The Global Colors of Psychropotes! 

So, here's the result. Scientists use diagrams to show a basic outline of relationships between different populations. Roughly speaking, the greater the distance between the circles the larger the distance between the populations and the greater chance they are separate species...

In the first diagram, the LARGER the circle, the larger the sample size. So the bigger circle represents the largest number of samples. Which were all from the Atlantic Ocean.  

Note the helpful color key so you can tell apart the populations you are seeing below:

Dark Blue= North Atlantic (east)                      

Light Blue= North Atlantic (west)

Yellow= South Indian Ocean

Green= South Atlantic

Red= Northeast Pacific 

Dark Purple= Northwest Pacific

Pink= South Pacific                                                                                               

    

Their figure 2 here shows what is basically the number of "steps" away from one another each population happens to be... The size of each circle represents the sample size. The big patch of BLUE reflects the LARGE sample of ATLANTIC specimens..but note how they are all clustered together. 

Some closer, some farther away.. This means they are all more closely related to one another than to those the others.  But note how many different subgroups are present away from the big blue circle in the middle?  That suggests lots of 

The Red (Northeast and Northwest Pacific) therefore seem to display a somewhat closer relationship to those in the North Atlantic than to those in the Southern hemisphere (yellow, green, pink, etc.)

Figure 2 from Gubili et al. 2016

Their figure 3 below, shows all of the populations in more of a "family tree" (i.e. phylogenetic) perspective..so, not only do we see that all of the Atlantic and Pacific members are "close" but they all occur on a single lineage, which means they were all MUCH more closely related

Two major lineages are most evident in the phylogenetic tree below, Lineages 1 and 2 each with subgroups:  Lin 1A, Lin 1B and Lin 2A and 2B, respectively. 

The pattern is kind of unclear..but there's definitely an Atlantic cluster (Lineage 2) with members that occur in the Indian and Pacific but this seems very separate from the Lineage 1 which seems to include members from all over, including the Indian Ocean and the South Pacific.

Figure 3 from Ghibili et al. 

Ultimately, the two lineages (Lineages 1 and 2) showed > 5% divergence from one another. When compared with other echinoderm species, that much population genetic divergence is enough to recognize a separate species (as opposed to simply a population with structure).

So, YES. One lineage, is the "proper" Psychropotes longicauda species, but there's at LEAST one more which has been "hidden" by the taxonomic definition of Psychropotes longicauda. That is, they all LOOK like the described species but in fact, the differences are FAR more subtle than we had previously recognized! More diversity (i.e., further species) will likely be discovered as more data is collected..

Some of these further subgroups will be so-called "cryptic species" because morphology does not immediately distinguish them. Thus, their status as species is "hidden" by external morphology (but subsequently discovered by genetics).  But now that we are looking, many, MANY more characters that could help distinguish these species could conceivably be discovered.

Other Interesting Observations/Questions..

One interesting factoid was that Psychropotes, and many other deep-sea sea cucumbers only occur in areas of high productivity (i.e. marine snow). Could these nutrient rich regions be related to speciation? and diversity within the species? 

                                      

The authors were able to note changes in the genetic diversity and abundance of the Atlantic lineage across a temporal series! Based on the extensive collections at the National Oceanography Collection at Southampton University, they they observed an uptick in the abundance of small individuals but also a change in the amount of genetic diversity  in relation to an increase in organic flux called the "Amperima Event" in 1996!

They found that there were MORE individuals which belonged to the "Atlantic population" and fewer of those which shoed affinities to other oceans. This might explain why the Atlantic "genetic type" was so well established.  They cautioned that although they didn't have enough of a dataset to show changes over time, they DID say that there WERE changes in the genetic makeup related to the nutrient availability. 

That is a pretty snazzy thing to record from a collection of deep-sea sea cucumbers! 

Is there an Antarctic origin for Psychropotes longicauda? 

The authors argue that the combination of Southern Indian Ocean lineages was consistent with other hypotheses arguing for an Antarctic origin for this widely occurring deep-sea sea cucumber. 

Repeated colonization events from the Antarctic via the Southern Indian Ocean (yellow colored in the figures above)  might explain the many lineages of Psychropotes present throughout the world's oceans as well as the presence of multiple lineages of Indian Ocean Psychropotes versus the derived and consistent clustering of Atlantic and Pacific populations.

(Coincidentally this picture of a Southern Atlantic Psychropotes is yellow!! )

http://archives.starbulletin.com/2007/06/24/news/story02.html

What further mysteries does Psychropotes have in store? I anxiously await the next paper! 

....now if I could only figure out what the "potes" part of Psychropotes means!

And just because, here are some FANTASTIC Psychropotes Bonuses! 

Here was an AWESOME Psychropotes cake by Elizabeth Ross, one of the authors of the study...

I had amazing office mates! Psychropotes longicauda cake and Deima validum meringues! @echinoblog pic.twitter.com/FHqExLTZ

— Libby Ross (@Libby_Ross) January 27, 2013

And of course Psychropotes stuffed animals.. from Japan of course!! 

from ebay http://www.ebay.com/itm/Psychropotes-varipes-Stuffed-Toy-sea-cucumber-peluches-Kuscheltiere-Japan-Eboshi-/271795943477