Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2022 Nov 29:10:e14414.
doi: 10.7717/peerj.14414. eCollection 2022.

The evolution of unique cranial traits in leporid lagomorphs

Affiliations

The evolution of unique cranial traits in leporid lagomorphs

Amber P Wood-Bailey et al. PeerJ. .

Abstract

Background: The leporid lagomorphs (rabbits and hares) are adapted to running and leaping (some more than others) and consequently have unique anatomical features that distinguish them from ochotonid lagomorphs (pikas) and from their rodent relatives. Two traits that have received some attention are fenestration of the lateral wall of the maxilla and facial tilting. These features are known to correlate with specialised locomotory form in that the faster running species will generally have fenestration that occupies the dorsal and the anteroventral surface of the maxillary corpus and a more acute facial tilt angle. Another feature is an intracranial joint that circumscribes the back of the skull, thought to facilitate skull mobility. This joint separates the anterior portion of the cranium (including the dentition, rostrum and orbit) from the posterior portion of the cranium (which encompasses the occipital and the auditory complex). Aside from the observation that the intracranial joint is absent in pikas (generalist locomotors) and appears more elaborate in genera with cursorial and saltatorial locomotory habits, the evolutionary history, biomechanical function and comparative anatomy of this feature in leporids lacks a comprehensive evaluation.

Methodology: The present work analysed the intracranial joint, facial tilting and lateral fenestration of the wall of the maxilla in the context of leporid evolutionary history using a Bayesian inference of phylogeny (18 genera, 23 species) and ancestral state reconstruction. These methods were used to gather information about the likelihood of the presence of these three traits in ancestral groups.

Results: Our phylogenetic analyses found it likely that the last common ancestor of living leporids had some facial tilting, but that the last common ancestor of all lagomorphs included in the dataset did not. We found that it was likely that the last common ancestor of living leporids had fenestration that occupies the dorsal, but not the anteroventral, surface of the maxillary corpus. We also found it likely that the last common ancestor of living leporids had an intracranial joint, but that the last common ancestor of all living lagomorphs did not. These findings provide a broader context to further studies of evolutionary history and will help inform the formulation and testing of functional hypotheses.

Keywords: Ancestral states; Cranial kinesis; Fossil mammals; Hares; Intracranial joint; Morphology; Phylogenetics; Rabbits; Skulls.

PubMed Disclaimer

Conflict of interest statement

The authors declare that they have no competing interests

Figures

Figure 1
Figure 1. Morphological characters added to the matrix developed by Meng, Hu & Li (2003), Asher et al. (2005) and Rose et al. (2008).
(A–C) The angle of the upper diastema to the line of the occipital plane is shown here on example Ochotona, Caprolagus and Lepus specimens to illustrate the three states in this character. In Ochotona, there is no facial tilting of note (state 0), in Caprolagus, there is moderate facial tilting (state 1) and in Lepus, there is more extreme facial tilting (state 2). (D–F) The morphological differences in maxillary fenestration are shown in Ochotona, Caprolagus and Lepus. In Ochotona, a single vacuity appears in the posterodorsal part of the maxillary corpus, highlighted in red (state 0), in Caprolagus, a latticework of small openings are restricted to the dorsal part of the maxillary corpus, highlighted in orange (state 1) and, in Lepus, fenestrations are located in the dorsal as well as the anteroventral surface of the maxillary corpus, highlighted in yellow (state 2). (G) The intracranial joint can be seen here between the supraoccipital and parietal bones in the lateral and posterior view, between the basioccipital and basisphenoid in the ventral view. In non-leporid lagomorphs, the joint is not present.
Figure 2
Figure 2. The phylogenetic hypotheses of extant Lagomorpha.
(A) Adapted from Matthee et al. (2004), (B) Ge et al. (2015) and (C) our phylogeny.
Figure 3
Figure 3. Ancestral state reconstruction of facial tilt.
All species within the range of the orange line are within Lagomorpha, within the blue line are within Leporidae and within the green line are within Ochotonidae. Red in the nodal markers refers to an obtuse facial tilt (as in extant Ochotona), yellow refers to a moderate facial tilt (as in Caprolagus) and orange refers to an extreme facial tilt (as in most Lepus).
Figure 4
Figure 4. Ancestral state reconstruction of fenestration of the lateral wall of the maxilla.
All species within the range of the orange line are within Lagomorpha, within the blue line are within Leporidae and within the green line are within Ochotonidae. Red in the nodal markers refers to a single vacuity (as in extant Ochotona), yellow refers to fenestration above the line of the bony remnant of the lacrimal duct (as in Lepus americanus) and orange refers to fenestration above and below the line of the bony remnant of the lacrimal duct (as in Lepus californicus).
Figure 5
Figure 5. Ancestral state reconstruction of the presence of an intracranial joint.
All species within the range of the orange line are within Lagomorpha, within the blue line are within Leporidae and within the green line are within Ochotonidae. Red in the nodal markers refers to the absence of an intracranial joint (as in all ochotonids). Orange refers to the presence of an intracranial joint (as in all leporids).

References

    1. Asher RJ, Meng J, Wible JR, McKenna MC, Rougier GW, Dashzeveg D, Novacek MJ. Stem lagomorpha and the antiquity of Glires. Science. 2005;307:1091–1094. doi: 10.1126/science.1107808. - DOI - PubMed
    1. Bailleul AM, Witmer LM, Holliday CM. Cranial joint histology in the mallard duck (Anas platyrhynchos); new insights on avian cranial kinesis. Journal of Anatomy. 2016;230(3):444–460. doi: 10.1111/joa.12562. - DOI - PMC - PubMed
    1. Barba-Montoya J, Tao Q, Kumar S. Molecular and morphological clocks for estimating evolutionary divergence times. BMC Ecology and Evolution. 2021;21:83. doi: 10.1186/s12862-021-01798-6. - DOI - PMC - PubMed
    1. Blanke A, Watson PJ, Holbrey R, Fagan MJ. Computational biomechanics changes our view on insect head evolution. Proceedings of the Royal Society B: Biological Sciences. 2017;284:20162412. doi: 10.1098/rspb.2016.2412. - DOI - PMC - PubMed
    1. Bleefeld AR, Bock WJ. Unique anatomy of lagomorph calcaneous. Acta Palaeontologica Polonica. 2002;47(1):181–183.

Publication types

LinkOut - more resources