Chondrocranial development in larval Rana sylvatica (Anura: Ranidae): Morphometric analysis of cranial allometry and ontogenetic shape change

Abstract

This study provides baseline quantitative data on the morphological development of the chondrocranium in a larval anuran. Both linear and geometric morphometric methods are used to quantitatively analyze size-related shape change in a complete developmental series of larvae of the wood frog, Rana sylvatica. The null hypothesis of isometry was rejected in all geometric morphometric and most linear morphometric analyses. Reduced major axis regressions of 11 linear chondrocranial measurements on size indicate a mixture of allometric and isometric scaling. Measurements in the otic and oral regions tend to scale with negative allometry and those associated with the palatoquadrate and muscular process scale with isometry or positive allometry. Geometric morphometric analyses, based on a set of 11 chondrocranial landmarks, include linear regression of relative warp scores and multivariate regression of partial warp scores and uniform components on log centroid size. Body size explains about one-quarter to one-third of the total shape variation found in the sample. Areas of regional shape transformation (e.g., palatoquadrate, otic region, trabecular horns) are identified by thin-plate spline deformation grids and are concordant with linear morphometric results. Thus, the anuran chondrocranium is not a static structure during premetamorphic stages and allometric patterns generally follow scaling predictions for tetrapod cranial development. Potential implications regarding larval functional morphology, cranial development, and chondrocranial evolution in anurans are discussed.

Geometric morphometrics in herpetology: modern tools for enhancing the study of morphological variation in amphibians and reptiles

“…pre-metamorphic shape ontogeny of the chondrocranium in anurans seems to generally follow a common pattern, at least in species of the genera Bufo, Pelodytes, Rana and Telmatobius (LArSon 2002(LArSon , 2004(LArSon , 2005cAnDIoTI, 2008;GArrIGA & LLorEnTE, in press). In these anuran species, general patterns of skull development include the reduction of the sensory capsules and a hypermetric or isometric growth of trophic structures (LArSon, 2002(LArSon, , 2004, in line with predictions made for all tetrapods (EMErSon & BrAMBLE, 1993). Interestingly, these studies also attest that the development of the chondrocranium does not seem to be tightly linked to that of the hind limb, thus rendering Gosner stages -a developmental staging system frequently used in anurans (GoSnEr, 1960) -a relatively poor indicator of chondrocranial differentiation (LArSon, 2002).…”

The importance of cartilage to amphibian development and evolution

“…Cartilages that are bent or compressed by loading are likely to experience changes in fluid pressure evenly throughout the tissue. Suggestions that the growth allometries of parts of tadpole chondrocrania reflect ontogenetic changes in mechanical loading (Larson, 2002) and that intraspecific differences in these allometries arise from food differences (Larson, 2004) are difficult to test. Tadpole chondrocranial growth appears to be affected by temperature (Jorgensen and Sheil, 2008), but given the daily extremes in temperature and unpredictable seasonal changes that most temperate amphibian larvae experience, it is difficult to envision skull cartilages effecting an adaptive response to this environmental variable in the way that limb cartilages do in endotherms (Serrat, 2014).…”

“…Parts of the chondrocranium that do not move and either disappear at metamorphosis, pass through it unchanged or serve as a framework for adding on new adult skeleton are expected to be more variable and more open to allometric growth. Both predictions are born out by the few morphometric studies currently available for tadpole skull development (Larson, 2002, Larson, 2004, Larson, 2005, Rose, 2015.…”

Osteologia e morfologia do condrocrânio de Gastrophryne carolinensis (Anura: Microhylidae), com uma revisão da diversidade osteológica dos Microhylidae do Novo Mundo.

“…In most other anuran larvae, which lack a posterolateral process, the chondrocranium at the posterior level of the palatoquadrate is about equal in width, or only slightly wider, than the width at the level of the muscular process, and the greatest width may be at the mid-orbital level (e.g., Lithobates sylvaticus [Larson 2002; Rana sylvatica auctorum] or Anaxyrus americanus [Larson 2004; Bufo americanus auctorum]). The frontoparietal fontanelle (and cranial cavity) in gastrophrynine and microhyline taxa tends to be short and wide, and the muscular process of the palatoquadrate poorly developed.…”