The Captorhinidae: herbivory and rates of evolutionary change

Dr. Neil Brocklehurst brings new insight to herbivory and evolution as he
compares rates of evolution as reptiles venture into a previously unexploited diet: plants. I did not comment on PeerJ where it is currently published without peer review because I thought it would be better here and Dr. Broklehurst reads this blog.

From the Brocklehurst abstract:
“Here I examine the impact of diet evolution on rates of morphological change in one of the earliest tetrapod clades to evolve high-fibre herbivory: Captorhinidae. Using a method of calculating heterogeneity in rates of discrete character change across a phylogeny, it is shown that a significant increase in rates of evolution coincides with the transition to herbivory in captorhinids.”

Brocklehurst notes
“By the end of the Cisuralian (Early Permian), five tetrapod lineages had independently evolved a herbivorous diet (referencing Sues and Riesz 1998).”

1. Captorhinidae
2. Diadectidae
3. Pareiasauridae
4. Caseidae
5. Edaphosauridae

Matching the Brocklehurst cladograms
In the LRT the basal herbivore is also Thuringothyris, and it nests close to the base of the new Lepidosauromorpha (Fig. 1) at the base of the Captorhinidae. One wonders if the original dichotomy of reptiles actually separated slightly larger herbivores from slightly smaller insectivores in the Viséan (Early Carboniferous)?  At present evidence only supports a later adoption of herbivory in the Late Carboniferous among several lepidosauromorph taxa. So there had to have been an earlier undiscovered origin. In any case the first four clades in the Sues and Riesz list (above green) are all related to each other in the clade Lepidosauromorpha. They all had a single ancestor (see below). Later lepidosauromorphs, like turtles, lizards, snakes and pterosaurs reacquired insectivory, piscivory and carnivory independently.

Late survivors of an earlier radiation
Urumqia (Fig. 3) nests as the basalmost lepidosauromorph, but fossils have only been found in Late Permian strata. Thus, Urumqia was a living fossil in the late Permian. Notably the gastralia were much wider than the posterior dorsal ribs. This created a large gut, ideal for herbivory (see below), but it also provided a larger volume for greater egg production.  Bruktererpeton was a sister and a basal lepidosauromorph with fossils found in Late Carboniferous strata with no obvious herbivorous traits. However, it too, nested with Thuringothyris (Fig. 1), so could have been an herbivore.

The taxon list
(Fig. 2) of Brocklehurst 2017 was restricted to his list of Captorhinidae. The LRT (Fig. 1) also nests most of his taxa within a single clade. However, Thuringothyris nests outside the Captorhinidae in the LRT but at its base. Saurorictus nests as the basal captorhinid in the LRT, despite its late appearance in the fossil record. It shares many traits with Millerettidae, a more derived taxon leading to all later lepidosauromorphs. Opisthodontosaurus appears in both cladograms, but its sister, Cephalerpeton appears only in the LRT. I have not yet seen data on Rhiodenticulatus and the derived captorhinid taxa are not present in the LRT. Limnoscelis and Orobates also nest as sisters to Saurorictus in the LRT. Limnoscelis is traditionally considered a carnivore, but since it is phylogenetically bracketed by herbivores, that hypothesis should be reexamined.

Sues and Reisz 1998 note:
“Dental features indicative of herbivorous habits include the presence of crushing and grinding dentitions, or marginal teeth with leaf-shaped, cuspidate crowns suitable for puncturing and shredding. Cranial features include short tooth rows and elevation or depression of the jaw joint for increased mechanical advantage during biting, large adductor chambers and deep lower jaws for accommodating large adductor jaw muscles, and jaw joints that permit fore-and-aft motion of the mandible.”

“The discovery of gut contents composed of conifer and pteridosperm ovules in specimens of the Late Permian diapsid reptile Protorosaurus (Munk and Sues 1992), long thought to be carnivorous based on its dentition, demonstrates that the consumption of plant material is not necessarily reflected by dental specialization.”

“The rib-cages of Palaeozoic herbivores are typically significantly wider and more capacious than those of their closest faunivorous relatives.”

Brocklehurst discusses rate variation:
“Discrete morphological character scores may be taken from the matrices used in cladistic analyses, and ancestral states are deduced using likelihood. This allows the number of character changes along each branch to be counted, and rates of character change are calculated by dividing the number of changes along a branch by the branch length. The absolute value calculated for the rate of each branch, however, can be misleading due to the presence of missing data (Lloyd et al. 2012). As such it is more useful to identify branches and clades where the rates of character change are significantly higher or lower than others, rather than comparing the raw numbers.”

Brocklehurst concludes:
“the evidence supporting an adaptive radiation of captorhinids coinciding with the origin of herbivory in this clade is compelling. It is only along herbivorous branches that significant increases in rates of morphological evolution are identified in the majority of the 100 time-calibrated trees.”

Brocklehurst has a good hypothesis with broader implications:
Among mammals, with the exception of tenrecs that turned into odontocete whales, the carnivores are more conservative than the herbivores, which developed horns, trunks and antlers, along with a variety of tooth morphologies. The clade Carnivora is quite conservative.

Among dinosaurs, with the exception of birds, the theropods are more conservative that the herbivores, which developed horns, long necks, great size, frills and duckbills.

Among reptiles, the lepidosauromorph herbivores developed into a wider variety of shapes and sizes while the archosauromorph insectivores were more conservative and stayed small until the advent of the lateral temporal fenestra that appeared in basal synapsids and diapsids.

References
Brocklehurst N 2017. Rates of morphological evolution in Captorhinidae: an adaptive radiation of Permian herbivores PeerJ Preprints (not peer-reviewed) PDF
Munk W and Sues H-D 1992. Gut contents of Parasaurus (Pareiasauria) and Protorosaurus (Archosauromorpha) from the Kupferschiefer (Upper Permian) of Hessen, Germany, Paläont. Z. 67, 169–176.
Sues H-D and Reisz RR 1998. Origins and early evolution of herbivory in tetrapods. Trends in Ecology and Evolution 13:141-145.

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