Limits...
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.


Contribution of the toothless extensions to heterochronic jaw growth in representatives of the Belonoidei. Alcian blue/alizarin red staining indicates that needlefish (B. belone) and halfbeak (D. pusilla) have toothless extensions of the lower jaw that are not present in medaka (O. latipes). (A, C, E), lateral orientation, (B, D, F) ventral orientation; age matched representatives, including (A, B) 28 dph medaka, O. latipes, (C, D) 7 dpb halfbeak, D. pusilla, (E, F) 6 dph needlefish, B. belone. Abbreviations: bl = body length, e = eye, lj = lower jaw, ljb = lower jaw basis, te = toothless extensions, uj = upper jaw.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3927394&req=5

Figure 3: Contribution of the toothless extensions to heterochronic jaw growth in representatives of the Belonoidei. Alcian blue/alizarin red staining indicates that needlefish (B. belone) and halfbeak (D. pusilla) have toothless extensions of the lower jaw that are not present in medaka (O. latipes). (A, C, E), lateral orientation, (B, D, F) ventral orientation; age matched representatives, including (A, B) 28 dph medaka, O. latipes, (C, D) 7 dpb halfbeak, D. pusilla, (E, F) 6 dph needlefish, B. belone. Abbreviations: bl = body length, e = eye, lj = lower jaw, ljb = lower jaw basis, te = toothless extensions, uj = upper jaw.

Mentions: Shortly after birth/hatching, halfbeak and needlefish display two rostrally-oriented outgrowths of the dentaries at their rostro-median contact zones (Figure 2 F, Figure 3C-F, Additional file5: Figure S3). The dentary outgrowths continue to extend throughout development and do not bare any teeth, even in mature adult stages (Figure 2 F-H, data not shown). Hence, they will hereon be referred to as ‘toothless extensions’. At early developmental stages, the toothless extensions do not stain with alizarin red, and only faintly with alcian blue, which is not visible in stained histological sections (Additional file5: Figure S3). The toothless extensions become progressively more ossified throughout development in a proximo-distal direction, (Figure 2 F-H, Additional file5: Figure S3), however the distal tips remain unossified even in adults (Figure 2G-H, data not shown)[47,50].


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)

Contribution of the toothless extensions to heterochronic jaw growth in representatives of the Belonoidei. Alcian blue/alizarin red staining indicates that needlefish (B. belone) and halfbeak (D. pusilla) have toothless extensions of the lower jaw that are not present in medaka (O. latipes). (A, C, E), lateral orientation, (B, D, F) ventral orientation; age matched representatives, including (A, B) 28 dph medaka, O. latipes, (C, D) 7 dpb halfbeak, D. pusilla, (E, F) 6 dph needlefish, B. belone. Abbreviations: bl = body length, e = eye, lj = lower jaw, ljb = lower jaw basis, te = toothless extensions, uj = upper jaw.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: Contribution of the toothless extensions to heterochronic jaw growth in representatives of the Belonoidei. Alcian blue/alizarin red staining indicates that needlefish (B. belone) and halfbeak (D. pusilla) have toothless extensions of the lower jaw that are not present in medaka (O. latipes). (A, C, E), lateral orientation, (B, D, F) ventral orientation; age matched representatives, including (A, B) 28 dph medaka, O. latipes, (C, D) 7 dpb halfbeak, D. pusilla, (E, F) 6 dph needlefish, B. belone. Abbreviations: bl = body length, e = eye, lj = lower jaw, ljb = lower jaw basis, te = toothless extensions, uj = upper jaw.
Mentions: Shortly after birth/hatching, halfbeak and needlefish display two rostrally-oriented outgrowths of the dentaries at their rostro-median contact zones (Figure 2 F, Figure 3C-F, Additional file5: Figure S3). The dentary outgrowths continue to extend throughout development and do not bare any teeth, even in mature adult stages (Figure 2 F-H, data not shown). Hence, they will hereon be referred to as ‘toothless extensions’. At early developmental stages, the toothless extensions do not stain with alizarin red, and only faintly with alcian blue, which is not visible in stained histological sections (Additional file5: Figure S3). The toothless extensions become progressively more ossified throughout development in a proximo-distal direction, (Figure 2 F-H, Additional file5: Figure S3), however the distal tips remain unossified even in adults (Figure 2G-H, data not shown)[47,50].

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.