Sunday, May 13, 2012

Parallel evolution in gigantic teleosts and baleen whales: filling the filter feeding niche during the Mesozoic

When people usually think of gigantic filter feeding critters in the sea, most people think of humpback whales - and the general group of marine mammals that I work on. Few marine mammal biologists could tell you much from a deep time perspective on the evolution of large filter feeding marine vertebrates - and few paleontologists in general even think about other marine organisms occupying a similar niche. In the oceans today, we also have a number of gigantic filter feeding sharks- the megamouth shark, discovered only in the late 1970's (Megachasma pelagios), the basking shark (Cetorhinus maximus), the whale shark (Rhincodon typus), and the manta ray (Manta birostris). Each of these groups (Mobulidae, Cetorhinus, Rhincodontidae, and Megachasmidae) all have relatively deep roots: early filter feeding devil rays and whale shark-like elasmobranchs are known from the Paleocene, and basking sharks from the Eocene. Megamouth sharks are known from the Pliocene and Miocene, and I am aware of some specimens in UCMP collections from the Oligocene and Miocene of Oregon. In 2007, Kenshu Shimada reidentified a tooth from the Cretaceous Greenhorn Fm. of Colorado he had originally published as Johnlongia sp. as a megamouth, and named it Megachasma comanchensis - which at the time was fascinating, because this was the first (possible) fossil record of a filter feeding shark prior to the Cenozoic. Baleen whales would not evolve until the latest Eocene.
The holotype and paratype teeth of Megachasma comanchensis, from Shimada 2007.


This has been an issue, because many researchers have noted or at least wondered about why the Mesozoic seas seemed to be devoid of gigantic filter feeders. Certainly, we know from the fossil record that there was no shortage of planktonic organisms to gulp up. How else could food webs be so drastically different between the Cretaceous and Paleogene? Nobody had a clear answer, and thus far it doesn't really look like any marine reptile we know of was really evolving towards a gigantic filter feeding ecology (there is one exception, the southern plesiosaur Aristonectes, which has a lot of tiny teeth that could have functioned as a sieve, and has generally been interpreted as a filter feeder). It was something I thought quite a bit about over the last few years - and to know avail. Aside from this Cretaceous species of Megachasma, the gigantic fish Leedsichthys was well known to be a gigantic (~10m) filter feeding teleost- but that was one genus known from a few fossils in the Jurassic.

 A depiction of Leedsichthys problematicus by Ray Troll.

In February 2010, I was fairly excited (about as excited I can get for anything older than the Paleogene...) a new article published in Science by Matt Friedman and others, publishing several new genera and records of other gigantic filter feeding pachycormid fishes, similar to Leedsichthys, and from numerous continents. These included Rhinconichthys from the Lower Chalk (Upper Cretaceous) of the southeastern UK,
an unidentifed toothless pachycormid from the Inferior Oolite (Upper Jurassic) of Dorset in the southwestern UK (for American readers - Dorset is a county along the southern coast of England, and is the home of Lyme Regis and the famed Mary Anning - along with being the setting of Jane Austen's novel Persuasion, and the setting of the book and movie The French Lieutenant's Woman starring Jeremy Irons and Meryl Streep, but I digress). They also reported the much better preserved Bonnerichthys from the Upper Cretaceous Niobrara Chalk in Kansas, and a Rhinconichthys-like fossil from the Upper Cretaceous Yezo Group of Hokkaido, Japan. Importantly, they identified fossils of this taxa from three different continents, indicating they were very geographically widespread. Secondly - and most importantly - they documented that these poorly known fishes were not just known from the Late Jurassic - but from the Middle Jurassic until the close of the Cretaceous.


The new stratigraphic range of known pachycormid fishes on the left (Figure 3 from Friedman et al. 2010) and the skull and partial skeleton of Bonnerichthys (Figure 2 from Friedman et al. 2010).


Interestingly, the fossil record now appeared to show that from the Jurassic onwards, that gigantic filter feeding vertebrates had continuously inhabited the earth's oceans until the present day. Prior to this study, the big question had been "Why did Mesozoic oceans lack abundant gigantic filter feeders?" I'll continue the dialogue by asking the opposite: Say we didn't have these, and with a hypothetically much better sampled record, had concluded the Mesozoic did not have any gigantic filter feeders. What sort of hypothetical situation could cause that? This may seem like a nonsensical and arbitrary question to ask, but I'll remind you that we don't really have any large Triassic filter feeders. I don't necessarily have an answer - but, one could easily surmise that there are a ton of morphological adaptations needed in order to even try filter feeding. Whatever morphology you start with is probably going to be something like piscivory - catching individual fish (or, crustaceans or cephalopods if you like). It's difficult to go from raptorial feeding to bulk feeding, and once a taxon is in a committed filter feeding niche - it's probably a one-way ticket; it is pretty hard to catch fast and maneuverable single prey items with a slow-closing mouth the size of pickup truck (Humpback whales do catch fish, and accidentally birds- but fish catching is simply done the same way they commit krill genocide). Some adaptations for filter feeding can probably be categorized as evolutionary 'ratchets' - development of a straining apparatus, and loss (or reduction) of teeth, both of which characterize all groups of gigantic filter feeding marine vertebrates. It is a little more clear-cut with fish, which already have a filtering apparatus needing little modification, and many fish already filter feed even at small body sizes, such as salmon; but for marine tetrapods, a really serious facelift needs to be performed, as teeth by themselves are not as efficient as, say, baleen is. This transition may necessitate some pretty weird transitional exaptations - we're still unclear on how baleen whales did it, for one. There have been and will be many more papers published on this particular topic, hopefully some from myself (regarding eomysticetids).

A painting of Bonnerichthys, an elasmosaurid, and some cephalopods by Robert Nicholls.

A more recent study by Matt Friedman (2011) expanded more on the evolution of pachycormiform fishes, and reinterpreted the Lower Jurassic fish Ohmdenia (from the Posidonia Shale of Germany) as an early pachycormiform, preserving an intermediate morphology between the ancestral condition and the derived, gigantic filter feeding condition. Derived pachycormiforms are toothless, with elongate, narrow jaws and a very large oral cavity, along with gigantic size. Ohmdenia also bore an elongate jaw, was relatively large (~2.5 m), but, like other basal pachycormiforms - retained a dentition. Its dentition had been reduced to a series of extremely tiny and stout teeth, which Friedman (2011) suggests were adapted for grasping soft bodied prey, rather than piercing the flesh of fish or other harder-bodied organisms. Two belemnites were found near the abdominal region of the skeleton of Ohmdenia, and these may represent gut contents- but the skeleton is disarticulated, so it is unclear if they arrived on the seafloor after the giant fish did. The elongate jaws of Ohmdenia also suggest comparatively weaker bite force than earlier pachycormiforms.


The holotype skeleton of the early pachycormiform fish Ohmdenia. From Friedman (2011).

To investigate the role of Ohmdenia in pachycormiform evolution, and to compare the evolution of filter feeding in these enigmatic fish and baleen whales, Friedman (2011) took a set of measurements reflecting various aspects of feeding in a number of different fossil and modern mysticetes, and pachycormiforms, and conducted a principal coordinates analysis. This allowed him to construct a "morphospace" - effectively, a field whose coordinates correspond to varying morphological characteristics (i.e. those which are measured by the researcher). A long while ago, in my Macroevolution course at MSU, we discussed the concept of "adaptive peaks" - regions of morphospace that are adaptive ideals; whether or not an organism or a clade achieves an adaptive peak, who knows - there are always circumstances that could preclude an organism from occupying some part of morphospace (i.e. anatomical constraints). Friedman's analysis showed that, interestingly - pachycormiforms and mysticetes, although originating at different regions of morphospace in the analysis - both converged onto the same adaptive peak. Furthermore, Friedman (2011) showed that in both cases, each group followed the same changes in this sequence: changes in dentition and mandibular geometry, loss of teeth, and evolution of giant body size. All in all, a rather impressive and fascinating study.
Phylogeny of pachycormiforms (A), transition of lower jaws in mysticetes and pachycormiforms (B), and morphospace analysis;  pachycormiforms in red, mysticetes in blue - solid circles = ancestral forms, triangles = Ohmdenia and transitional mysticetes, and open circles = filter feeding pachycormiforms and mysticetes, convering in the lower right hand corner (C). From Friedman (2011).


References-

Friedman, M. 2011.Parallel evolutionary trajectories underlie the origin of giant suspension-feeding whales and bony fishes. Proceedings of the Royal Society B: 279:944-951.

Friedman, M., Shimada, K., Martin, L.D., Everhart, M.J., Liston, J., Maltese, A., and Triebold, M. 2010. 100-Million-year dynasty of giant planktivorous bony fishes in the Mesozoic seas. Science 327:990-993.

Shimada, K. 2007. Mesozoic origin for megamouth shark (Lamniformes: Megachasmidae). Journal of Vertebrate Paleontology 27:512-516.

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