Facultative paedomorphosis and the pattern of intra- and interspecific variation in cranial skeleton: lessons from European newts (Ichthyosaura alpestris and Lissotriton vulgaris)

Ivanović, Ana; Cvijanović, Milena; Denoël, Mathieu; Slijepčević, Maja; Kalezić, Miloš L.

doi:10.1007/s00435-013-0202-7

Cited by 15 publications

(17 citation statements)

References 59 publications

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“…Eliminating TH produces zebrafish with highly reduced ascending arms and feeding mechanisms that resemble those of close relatives with nonprotrusile jaws (Table and Figures and ; S. McMenamin et al, ). Many of these have been described as being paedomorphic (Britz, Conway, & Rueber, ; Kullander & Britz, ), a condition that is strongly associated with changes in TH signaling in vertebrates (De Groef, Grommen, & Darras, ; Ivanovic, Cvijanovic, Denoel, Slijepcevic, & Kalezic, ; Laudet, ). Differences in jaw protrusion ability are strongly associated with differences in diet in marine damselfishes (Cooper, McGraw, Khazanchi, & Ieee., ), and although diet data for wild danionins is limited or nonexistent, we suspect that the same may be true for the species examined here.…”

Section: Discussionmentioning

confidence: 99%

Thyroid hormone modulation during zebrafish development recapitulates evolved diversity in danionin jaw protrusion mechanics

Galindo

Sweet

DeLeon

et al. 2019

Evolution and Development

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Protrusile jaws are a highly useful innovation that has been linked to extensive diversification in fish feeding ecology. Jaw protrusion can enhance the performance of multiple functions, such as suction production and capturing elusive prey. Identifying the developmental factors that alter protrusion ability will improve our understanding of fish diversification. In the zebrafish protrusion arises postmetamorphosis. Fish metamorphosis typically includes significant changes in trophic morphology, accompanies a shift in feeding niche and coincides with increased thyroid hormone production. We tested whether thyroid hormone affects the development of zebrafish feeding mechanics. We found that it affected all developmental stages examined, but that effects were most pronounced after metamorphosis. Thyroid hormone levels affected the development of jaw morphology, feeding mechanics, shape variation, and cranial ossification. Adult zebrafish utilize protrusile jaws, but an absence of thyroid hormone impaired development of the premaxillary bone, which is critical to jaw protrusion. Premaxillae from early juvenile zebrafish and hypothyroid adult zebrafish resemble those from adults in the genera Danionella, Devario, and Microdevario that show little to no jaw protrusion. Our findings suggest that evolutionary changes in how the developing skulls of danionin minnows respond to thyroid hormone may have promoted diversification into different feeding niches.

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Section: Discussionmentioning

confidence: 99%

Thyroid hormone modulation during zebrafish development recapitulates evolved diversity in danionin jaw protrusion mechanics

Galindo

Sweet

DeLeon

et al. 2019

Evolution and Development

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“…The morphology of the skull and hyobranchial apparatus of metamorphosed and paedomorphic salamandrids is described in detail elsewhere [16–18, 20, 21, 32, 55, 62]; we focus mainly on the overall head morphology of both morphs and center on the hyobranchium and the rectus cervicis muscle system. Description and terminology largely follows Drüner [17, 18], Francis [21], Özeti and Wake [55], Findeis and Bemis [20].…”

Section: Resultsmentioning

confidence: 99%

“…Paedomorphosis is defined as the retention of juvenile characters in sexually mature adults and is common in many salamander groups. In paedomorphic salamanders, adults forego metamorphosis and retain larval characters, such as the larval skull, hyobranchial musculoskeletal system, external gills, gill slits and fin folds [22, 32, 43, 56, 57, 66]. Paedomorphosis evolved multiple times independently in salamanders and larval development can be arrested in different ontogenetic stages [22, 74].…”

Section: Introductionmentioning

confidence: 99%

Same but different: aquatic prey capture in paedomorphic and metamorphic Alpine newts

Heiss

Grell

2019

Zoological Lett

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Paedomorphosis describes the retention of larval characters in adult stages and is widespread amongst salamanders. Salamandrid newts exhibit facultative paedomorphosis, where paedomorphic and metamorphic adult forms coexist in the same population. Previous studies have shown that prey capture kinematics do not differ between paedomorphic and metamorphosed ambystomatid salamanders, despite diverging morphology and prey capture performance. It remained unclear, however, whether the stereotypy of prey capture kinematics across morphotypes is restricted to ambystomatids, or can be found in other salamander groups too. Here, we performed biplanar high-speed-recordings of the prey capture behavior in paedomorphic and metamorphic salamandrid newts and only found minor kinematic differences across morphotypes, suggesting that stereotypy across morphotypes is a more general feature within salamanders. We then compared anatomy of skull and hyobranchial skeleton, along with the physiological cross sectional area (PCSA) of the rectus cervicis muscle, the main muscle empowering suction feeding. Besides the overall morphological differences of the feeding apparatus, the PCSA of the rectus cervicis also differs significantly between morphotypes, being twice as large in paedomorphs. Accordingly, paedomorphs can exert more powerful suction strikes, which in turn may be one of the key factors why paedomorphs are more efficient in capturing elusive prey compared to metamorphs.

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“…Second, processing might be affected more from differing feeding apparatus morphologies than capture and transport. This latter point becomes more evident if we consider changes in the structure, position and number of the teeth [26][27][28][29]; structural changes of the hyobranchial apparatus (i.e., developing from a gill-bearing to a tongue-bearing apparatus) [14,15,[30][31][32]; changes in the muscular and ligamentous suspension of the hyobranchial apparatus [33][34][35]; morphological changes of mandible and skull [15,[36][37][38]; as well as dramatic muscular reorganization [39,40] during metamorphosis in salamanders. All of the aforementioned characteristics impact intraoral food processing kinematics in salamanders [21,23].…”

Section: Introductionmentioning

confidence: 99%

Ontogenetic plasticity in cranial morphology is associated with a change in the food processing behavior in Alpine newts

et al. 2020

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Background The feeding apparatus of salamanders consists mainly of the cranium, mandible, teeth, hyobranchial apparatus and the muscles of the cranial region. The morphology of the feeding apparatus in turn determines the boundary conditions for possible food processing (i.e., intraoral mechanical reduction) mechanisms. However, the morphology of the feeding apparatus changes substantially during metamorphosis, prompting the hypothesis that larvae might use a different food processing mechanism than post-metamorphic adults. Salamandrid newts with facultative metamorphosis are suitable for testing this hypothesis as adults with divergent feeding apparatus morphologies often coexist in the same population, share similar body sizes, and feed on overlapping prey spectra. Methods We use high-speed videography to quantify the in vivo movements of key anatomical elements during food processing in paedomorphic and metamorphic Alpine newts (Ichthyosaura alpestris). Additionally, we use micro-computed tomography (μCT) to analyze morphological differences in the feeding apparatus of paedomorphic and metamorphic Alpine newts and sort them into late-larval, mid-metamorphic and post-metamorphic morphotypes. Results Late-larval, mid-metamorphic and post-metamorphic individuals exhibited clear morphological differences in their feeding apparatus. Regardless of the paedomorphic state being externally evident, paedomorphic specimens can conceal different morphotypes (i.e., late-larval and mid-metamorphic morphotypes). Though feeding on the same prey under the same (aquatic) condition, food processing kinematics differed between late-larval, mid-metamorphic and post-metamorphic morphotypes. Conclusions The food processing mechanism in the Alpine newt changes along with morphology of the feeding apparatus during ontogeny, from a mandible-based to a tongue-based processing mechanism as the changing morphology of the mandible prevents chewing and the tongue allows enhanced protraction. These results could indicate that early tetrapods, in analogy to salamanders, may have developed new feeding mechanisms in their aquatic environment and that these functional innovations may have later paved the way for terrestrial feeding mechanisms.

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Facultative paedomorphosis and the pattern of intra- and interspecific variation in cranial skeleton: lessons from European newts (Ichthyosaura alpestris and Lissotriton vulgaris)

Abstract: Springer).

Cited by 15 publications

References 59 publications

Thyroid hormone modulation during zebrafish development recapitulates evolved diversity in danionin jaw protrusion mechanics

Thyroid hormone modulation during zebrafish development recapitulates evolved diversity in danionin jaw protrusion mechanics

Same but different: aquatic prey capture in paedomorphic and metamorphic Alpine newts

Ontogenetic plasticity in cranial morphology is associated with a change in the food processing behavior in Alpine newts

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