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Revisiting de Beer's textbook example of heterochrony and jaw elongation in fish: calmodulin expression reflects heterochronic growth, and underlies morphological innovation in the jaws of belonoid fishes.

Gunter HM, Koppermann C, Meyer A - Evodevo (2014)

Bottom Line: Heterochronic shifts during ontogeny can result in adaptively important innovations and might be initiated by simple developmental switches.Early in development, the lower jaw displays accelerated growth both in needlefish and halfbeak compared to medaka, and secondary acceleration of the upper jaw is seen in needlefish later in their development, representing a case of mosaic heterochrony.Our results suggest that calm1 contributes to jaw heterochrony in halfbeak, potentially driving further heterochronic shifts in jaw growth across the Suborder Belonoidei, such as the upper jaw acceleration observed in needlefish.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biology, Lehrstuhl für Zoologie und Evolutionsbiologie, University of Konstanz, Universitätstrasse 10, 78457 Constance, Germany. Axel.Meyer@uni-konstanz.de.

ABSTRACT

Background: Heterochronic shifts during ontogeny can result in adaptively important innovations and might be initiated by simple developmental switches. Understanding the nature of these developmental events can provide insights into fundamental molecular mechanisms of evolutionary change. Fishes from the Suborder Belonoidei display a vast array of extreme craniofacial morphologies that appear to have arisen through a series of heterochronic shifts. We performed a molecular heterochrony study, comparing postembryonic jaw development in representatives of the Suborder Belonoidei, the halfbeak Dermogenys pusilla (where the lower jaw is considerably elongated compared to the upper jaw) and the needlefish Belone belone (where both jaws are elongated), to a representative of their sister group the Suborder Adrianichthyoidei, the medaka Oryzias latipes, which has retained the ancestral morphology.

Results: Early in development, the lower jaw displays accelerated growth both in needlefish and halfbeak compared to medaka, and secondary acceleration of the upper jaw is seen in needlefish later in their development, representing a case of mosaic heterochrony. We identified toothless extensions of the dentaries as innovations of Belonoid fishes and the source of heterochronic growth. The molecular basis of growth heterochronies in the Belonoidei was examined through comparing expression of skeletogenic genes during development of halfbeak and medaka. The calmodulin paralogue calm1 was identified as a potential regulator of jaw length in halfbeak as its expression gradually increases in the lower jaw, but not the upper jaw, in a pattern that matches its outgrowth. Moreover, medaka displays equal expression of calm1 in the upper and lower jaws, consistent with the lack of jaw outgrowth in this species.

Conclusions: Heterochronic shifts in jaw growth have occurred repeatedly during the evolution of Belonoid fishes and we identify toothless extensions of the dentaries as an important innovation of this group. Our results suggest that calm1 contributes to jaw heterochrony in halfbeak, potentially driving further heterochronic shifts in jaw growth across the Suborder Belonoidei, such as the upper jaw acceleration observed in needlefish.

No MeSH data available.


Related in: MedlinePlus

Comparative skeletal development of medaka, Oryzias latipes and halfbeak, Dermogenys pusilla. (A-H) lateral orientation, (A-D) O. latipes, (E-H) D. pusilla, stages are matched based on the relative timing of skeletal ossification. The upper and lower jaws of medaka maintain roughly similar proportions throughout development (A-D). At birth, the jaws of halfbeak resemble those of medaka (E), however they become elongated throughout development, whereby the lower jaw grows proportionally more than the upper jaw (F-H). Abbreviations: den = dentary, dpb = days post birth, dph = days post hatch, e = eye, eth = ethmoid, lpj = lower pharyngeal jaw, mc = Meckel’s cartilage, mx = maxilla, pmx = premaxilla.
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Figure 2: Comparative skeletal development of medaka, Oryzias latipes and halfbeak, Dermogenys pusilla. (A-H) lateral orientation, (A-D) O. latipes, (E-H) D. pusilla, stages are matched based on the relative timing of skeletal ossification. The upper and lower jaws of medaka maintain roughly similar proportions throughout development (A-D). At birth, the jaws of halfbeak resemble those of medaka (E), however they become elongated throughout development, whereby the lower jaw grows proportionally more than the upper jaw (F-H). Abbreviations: den = dentary, dpb = days post birth, dph = days post hatch, e = eye, eth = ethmoid, lpj = lower pharyngeal jaw, mc = Meckel’s cartilage, mx = maxilla, pmx = premaxilla.

Mentions: The developmental basis of lower jaw extension was examined using histostaining, comparing needlefish and halfbeak development to that of medaka, with a particular focus on halfbeak and medaka due to their experimental tractability. As skeletal development has previously been described for these three species[47-49], aspects of skeletal development that related directly to growth heterochrony were the main focus of this study. Halfbeak and needlefish at birth and hatching respectively, displayed a similar jaw morphology to age matched medaka (Figure 2A and E, data not shown). One notable exception is that compared to medaka, the Meckel’s cartilages of halfbeak and needlefish display a shift in their posterior limits, corresponding to a posterior fusion of the angulo-articular to the dentaries in halfbeak and needlefish[47] (conversely, the angulo-articular is nested under the dentaries in medaka).


Revisiting de Beer's textbook example of heterochrony and jaw elongation in fish: calmodulin expression reflects heterochronic growth, and underlies morphological innovation in the jaws of belonoid fishes.

Gunter HM, Koppermann C, Meyer A - Evodevo (2014)

Comparative skeletal development of medaka, Oryzias latipes and halfbeak, Dermogenys pusilla. (A-H) lateral orientation, (A-D) O. latipes, (E-H) D. pusilla, stages are matched based on the relative timing of skeletal ossification. The upper and lower jaws of medaka maintain roughly similar proportions throughout development (A-D). At birth, the jaws of halfbeak resemble those of medaka (E), however they become elongated throughout development, whereby the lower jaw grows proportionally more than the upper jaw (F-H). Abbreviations: den = dentary, dpb = days post birth, dph = days post hatch, e = eye, eth = ethmoid, lpj = lower pharyngeal jaw, mc = Meckel’s cartilage, mx = maxilla, pmx = premaxilla.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3927394&req=5

Figure 2: Comparative skeletal development of medaka, Oryzias latipes and halfbeak, Dermogenys pusilla. (A-H) lateral orientation, (A-D) O. latipes, (E-H) D. pusilla, stages are matched based on the relative timing of skeletal ossification. The upper and lower jaws of medaka maintain roughly similar proportions throughout development (A-D). At birth, the jaws of halfbeak resemble those of medaka (E), however they become elongated throughout development, whereby the lower jaw grows proportionally more than the upper jaw (F-H). Abbreviations: den = dentary, dpb = days post birth, dph = days post hatch, e = eye, eth = ethmoid, lpj = lower pharyngeal jaw, mc = Meckel’s cartilage, mx = maxilla, pmx = premaxilla.
Mentions: The developmental basis of lower jaw extension was examined using histostaining, comparing needlefish and halfbeak development to that of medaka, with a particular focus on halfbeak and medaka due to their experimental tractability. As skeletal development has previously been described for these three species[47-49], aspects of skeletal development that related directly to growth heterochrony were the main focus of this study. Halfbeak and needlefish at birth and hatching respectively, displayed a similar jaw morphology to age matched medaka (Figure 2A and E, data not shown). One notable exception is that compared to medaka, the Meckel’s cartilages of halfbeak and needlefish display a shift in their posterior limits, corresponding to a posterior fusion of the angulo-articular to the dentaries in halfbeak and needlefish[47] (conversely, the angulo-articular is nested under the dentaries in medaka).

Bottom Line: Heterochronic shifts during ontogeny can result in adaptively important innovations and might be initiated by simple developmental switches.Early in development, the lower jaw displays accelerated growth both in needlefish and halfbeak compared to medaka, and secondary acceleration of the upper jaw is seen in needlefish later in their development, representing a case of mosaic heterochrony.Our results suggest that calm1 contributes to jaw heterochrony in halfbeak, potentially driving further heterochronic shifts in jaw growth across the Suborder Belonoidei, such as the upper jaw acceleration observed in needlefish.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biology, Lehrstuhl für Zoologie und Evolutionsbiologie, University of Konstanz, Universitätstrasse 10, 78457 Constance, Germany. Axel.Meyer@uni-konstanz.de.

ABSTRACT

Background: Heterochronic shifts during ontogeny can result in adaptively important innovations and might be initiated by simple developmental switches. Understanding the nature of these developmental events can provide insights into fundamental molecular mechanisms of evolutionary change. Fishes from the Suborder Belonoidei display a vast array of extreme craniofacial morphologies that appear to have arisen through a series of heterochronic shifts. We performed a molecular heterochrony study, comparing postembryonic jaw development in representatives of the Suborder Belonoidei, the halfbeak Dermogenys pusilla (where the lower jaw is considerably elongated compared to the upper jaw) and the needlefish Belone belone (where both jaws are elongated), to a representative of their sister group the Suborder Adrianichthyoidei, the medaka Oryzias latipes, which has retained the ancestral morphology.

Results: Early in development, the lower jaw displays accelerated growth both in needlefish and halfbeak compared to medaka, and secondary acceleration of the upper jaw is seen in needlefish later in their development, representing a case of mosaic heterochrony. We identified toothless extensions of the dentaries as innovations of Belonoid fishes and the source of heterochronic growth. The molecular basis of growth heterochronies in the Belonoidei was examined through comparing expression of skeletogenic genes during development of halfbeak and medaka. The calmodulin paralogue calm1 was identified as a potential regulator of jaw length in halfbeak as its expression gradually increases in the lower jaw, but not the upper jaw, in a pattern that matches its outgrowth. Moreover, medaka displays equal expression of calm1 in the upper and lower jaws, consistent with the lack of jaw outgrowth in this species.

Conclusions: Heterochronic shifts in jaw growth have occurred repeatedly during the evolution of Belonoid fishes and we identify toothless extensions of the dentaries as an important innovation of this group. Our results suggest that calm1 contributes to jaw heterochrony in halfbeak, potentially driving further heterochronic shifts in jaw growth across the Suborder Belonoidei, such as the upper jaw acceleration observed in needlefish.

No MeSH data available.


Related in: MedlinePlus