skip to main content


Title: Heterochronic Shifts Mediate Ecomorphological Convergence in Skull Shape of Microcephalic Sea Snakes
Abstract Morphological variation among the viviparous sea snakes (Hydrophiinae), a clade of fully aquatic elapid snakes, includes an extreme “microcephalic” ecomorph that has a very small head atop a narrow forebody, while the hind body is much thicker (up to three times the forebody girth). Previous research has demonstrated that this morphology has evolved at least nine times as a consequence of dietary specialization on burrowing eels, and has also examined morphological changes to the vertebral column underlying this body shape. The question addressed in this study is what happens to the skull during this extreme evolutionary change? Here we use X-ray micro-computed tomography and geometric morphometric methods to characterize cranial shape variation in 30 species of sea snakes. We investigate ontogenetic and evolutionary patterns of cranial shape diversity to understand whether cranial shape is predicted by dietary specialization, and examine whether cranial shape of microcephalic species may be a result of heterochronic processes. We show that the diminutive cranial size of microcephalic species has a convergent shape that is correlated with trophic specialization to burrowing prey. Furthermore, their cranial shape is predictable for their size and very similar to that of juvenile individuals of closely related but non-microcephalic sea snakes. Our findings suggest that heterochronic changes (resulting in pedomorphosis) have driven cranial shape convergence in response to dietary specializations in sea snakes.  more » « less
Award ID(s):
1839250
NSF-PAR ID:
10170988
Author(s) / Creator(s):
; ; ; ; ;
Date Published:
Journal Name:
Integrative and Comparative Biology
Volume:
59
Issue:
3
ISSN:
1540-7063
Page Range / eLocation ID:
616 to 624
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Crocodylomorpha, which includes living crocodylians and their extinct relatives, has a rich fossil record, extending back for more than 200 million years. Unlike modern semi‐aquatic crocodylians, extinct crocodylomorphs exhibited more varied lifestyles, ranging from marine to fully terrestrial forms. This ecological diversity was mirrored by a remarkable morphological disparity, particularly in terms of cranial morphology, which seems to be closely associated with ecological roles in the group. Here, I use geometric morphometrics to comprehensively investigate cranial shape variation and disparity in Crocodylomorpha. I quantitatively assess the relationship between cranial shape and ecology (i.e. terrestrial, aquatic, and semi‐aquatic lifestyles), as well as possible allometric shape changes. I also characterize patterns of cranial shape evolution and identify regime shifts. I found a strong link between shape and size, and a significant influence of ecology on the observed shape variation. Terrestrial taxa, particularly notosuchians, have significantly higher disparity, and shifts to more longirostrine regimes are associated with large‐bodied aquatic or semi‐aquatic species. This demonstrates an intricate relationship between cranial shape, body size and lifestyle in crocodylomorph evolutionary history. Additionally, disparity‐through‐time analyses were highly sensitive to different phylogenetic hypotheses, suggesting the description of overall patterns among distinct trees. For crocodylomorphs, most results agree in an early peak during the Early Jurassic and another in the middle of the Cretaceous, followed by nearly continuous decline until today. Since only crown‐group members survived through the Cenozoic, this decrease in disparity was likely the result of habitat loss, which narrowed down the range of crocodylomorph lifestyles.

     
    more » « less
  2. Abstract

    The fossil record provides compelling examples of heterochrony at macroevolutionary scales such as the peramorphic giant antlers of the Irish elk. Heterochrony has also been invoked in the evolution of the distinctive cranial frill of ceratopsian dinosaurs such asTriceratops. Although ceratopsian frills vary in size, shape, and ornamentation, quantitative analyses that would allow for testing hypotheses of heterochrony are lacking. Here, we use geometric morphometrics to examine frill shape variation across ceratopsian diversity and within four species preserving growth series. We then test whether the frill constitutes an evolvable module both across and within species, and compare growth trajectories of taxa with ontogenetic growth series to identify heterochronic processes. Evolution of the ceratopsian frill consisted primarily of progressive expansion of its caudal and caudolateral margins, with morphospace occupation following taxonomic groups. Although taphonomic distortion represents a complicating factor, our data support modularity both across and within species. Peramorphosis played an important role in frill evolution, with acceleration operating early in neoceratopsian evolution followed by progenesis in later diverging cornosaurian ceratopsians. Peramorphic evolution of the ceratopsian frill may have been facilitated by the decoupling of this structure from the jaw musculature, an inference that predicts an expansion of morphospace occupation and higher evolutionary rates among ceratopsids as indeed borne out by our data. However, denser sampling of the meager record of early‐diverging taxa is required to test this further.

     
    more » « less
  3. Abstract

    Size and shape are often considered important variables that lead to variation in performance. In studies of feeding, size‐corrected metrics of the skull are often used as proxies of biting performance; however, few studies have examined the relationship between cranial shape in its entirety and estimated bite force across species and how dietary ecologies may affect these variables differently. Here, we used geometric morphometric and phylogenetic comparative approaches to examine relationships between cranial morphology and estimated bite force in the carnivoran clade Musteloidea. We found a strong relationship between cranial size and estimated bite force but did not find a significant relationship between cranial shape and size‐corrected estimated bite force. Many‐to‐one mapping of form to function may explain this pattern because a variety of evolutionary shape changes rather than a single shape change may have contributed to an increase in relative biting ability. We also found that dietary ecologies influenced cranial shape evolution but did not influence cranial size nor size‐corrected bite force evolution. Although musteloids with different diets exhibit variation in cranial shapes, they have similar estimated bite forces suggesting that other feeding performance metrics and potentially nonfeeding traits are also important contributors to cranial evolution. We postulate that axial and appendicular adaptations and the interesting feeding behaviours reported for species within this group also facilitate different dietary ecologies between species. Future work integrating cranial, axial and appendicular form and function with behavioural observations will reveal further insights into the evolution of dietary ecologies and other ecological variables.

     
    more » « less
  4. Abstract

    Carnivorans represent extreme ecomorphological diversity, encompassing remarkable variation in form, habitat, and diet. The relationship between the masticatory musculature and dietary ecology has been explored in a number of carnivoran lineages, including felids and the superfamily Musteloidea. In this study, we present novel architectural data on two additional carnivoran families—Ursidae and Canidae—and supplement these previous studies with additional felid, musteloid, herpestid, hyaenid, and viverrid taxa (a total of 53 species across 10 families). Gross dissection data were collected following a standardized protocol—sharp dissection followed by chemical digestion. Summed jaw adductor forces were also transformed into bite force estimates (BF) using osteologically calculated leverages. All data were linearized, log‐transformed, and size‐adjusted using two proxies for each taxon—body mass (BM) and cranial geometric mean—to assess relative scaling trends. These architectural data were then analyzed in the context of dietary ecology to examine the impact of dietary size (DS) and dietary mechanical properties (DMP). Muscle mass, physiological cross‐sectional area, and BF scaled with isometry or positive allometry in all cases, whereas fascicle lengths (FLs) scaled with isometry or negative allometry. With respect to diet, BM‐adjusted FLs were strongly correlated with DS in musteloids, but not in any other lineage. The relationship between size‐adjusted BF and DMP was also significant within musteloids, and across the sample as a whole, but not within other individual lineages. This interfamilial trend may reflect the increased morphological and dietary diversity of musteloids relative to other carnivoran groups.

     
    more » « less
  5. Abstract

    Members of an ecological guild may be anticipated to show morphological convergence, as similar functional demands exert similar selective pressures on phenotypes. Nature is rife with examples, however, where such taxa instead exhibit ‘incomplete’ convergence or even divergence. Incorporating factors such as character displacement by other guild members or variation in ecological specialization itself may therefore be necessary to gain a more complete understanding of what constrains or promotes diversity. Cleaning, a behavior in which species remove and consume ectoparasites from “clientele,” has been shown to exhibit variation in specialization and has evolved in a variety of marine habitats around the globe. To determine the extent to which specialization in this tropic strategy has affected phenotypic evolution, we examined the evolution of cleaning behavior in five marine fish families: Labridae, Gobiidae, Pomacanthidae, Pomacentridae, and Embiotocidae. We used a comparative framework to determine patterns of convergence and divergence in body shape and size across non-cleaning and cleaning members within these five clades. Highly specialized obligate cleaning, found in the Indo-Pacific and the Caribbean, evolved in the Labridae and Gobiidae at strikingly similar times. In these two regions, obligate cleaning evolves early, shows convergence on an elongate body shape, and is restricted to species of small body size. Facultative cleaning, shown either throughout ontogeny or predominately in the juvenile phase, exhibits a much more varied phenotype, especially in geographic regions where obligate cleaning occurs. Collectively, our results are consistent with varying extents of an ecological specialization constraining or spurring morphological evolution in recurrent ways across regions.

     
    more » « less