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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.


Expression of calm paralogues during jaw outgrowth in medaka and halfbeak. (A-F) Expression of calm paralogues in (A-C) medaka and (D-F) halfbeak, including (A, D) calm1, (B, E) calm2, (C, F) calm3. Note, genes we denote medaka calm1, calm2 and calm3 have previously been denoted CaM-A, CaM-B and CaM-C, but we have re-named them due to the orthology relationships identified by our phylogenetic analysis. Relative expression values are scaled so that expression in the lower jaw of embryos = 1. Standard error is indicated. Two-way ANOVAs show a statistically significant difference in expression for calm1 in halfbeak (P < 0.001), but not medaka (P > 0.1). Neither calm2 nor calm3 show differential expression for halfbeak or medaka (P > 0.1) (see Table 1). RQ = relative quantitation.
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Figure 6: Expression of calm paralogues during jaw outgrowth in medaka and halfbeak. (A-F) Expression of calm paralogues in (A-C) medaka and (D-F) halfbeak, including (A, D) calm1, (B, E) calm2, (C, F) calm3. Note, genes we denote medaka calm1, calm2 and calm3 have previously been denoted CaM-A, CaM-B and CaM-C, but we have re-named them due to the orthology relationships identified by our phylogenetic analysis. Relative expression values are scaled so that expression in the lower jaw of embryos = 1. Standard error is indicated. Two-way ANOVAs show a statistically significant difference in expression for calm1 in halfbeak (P < 0.001), but not medaka (P > 0.1). Neither calm2 nor calm3 show differential expression for halfbeak or medaka (P > 0.1) (see Table 1). RQ = relative quantitation.

Mentions: The molecular basis of heterochronic growth was examined in halfbeak as a first step to determining the molecular basis of craniofacial diversity within the Belonoidei. The expression of candidate genes, including bmp2, bmp4, runx2, sox9b and three calmodulin orthologues, denoted calm1, calm2 and calm3 was compared between upper and lower jaws at a range of developmental stages that appear to be important for jaw outgrowth (Figure 5A, Additional file6: Figure S4, Additional file3: Table S2). We observed significantly differential expression for four of the seven genes examined, based on two-way ANOVAs (Table 1). The majority of genes in our study were upregulated in the lower jaw relative to the upper jaw - amongst these were sox9b, runx2 and calm1, while bmp2 was upregulated in the upper jaw (Figure 5B-D, Figure 6D). As both sox9b and runx2 were upregulated in the lower jaw, we infer that both chondrogenic (cartilage-forming) and osteogenic (bone-forming) pathways are required for the outgrowth of the lower jaw, presumably the result of their enhanced expression in Meckel’s cartilages and the dentaries respectively (Additional file3: Table S2). Expression of bmp2 was significantly higher in the upper jaw, which matches neither runx2 nor sox9b (Figure 5B-D), reducing the possibility that it is involved in either bone or cartilage development for the stages we examined.


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)

Expression of calm paralogues during jaw outgrowth in medaka and halfbeak. (A-F) Expression of calm paralogues in (A-C) medaka and (D-F) halfbeak, including (A, D) calm1, (B, E) calm2, (C, F) calm3. Note, genes we denote medaka calm1, calm2 and calm3 have previously been denoted CaM-A, CaM-B and CaM-C, but we have re-named them due to the orthology relationships identified by our phylogenetic analysis. Relative expression values are scaled so that expression in the lower jaw of embryos = 1. Standard error is indicated. Two-way ANOVAs show a statistically significant difference in expression for calm1 in halfbeak (P < 0.001), but not medaka (P > 0.1). Neither calm2 nor calm3 show differential expression for halfbeak or medaka (P > 0.1) (see Table 1). RQ = relative quantitation.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Figure 6: Expression of calm paralogues during jaw outgrowth in medaka and halfbeak. (A-F) Expression of calm paralogues in (A-C) medaka and (D-F) halfbeak, including (A, D) calm1, (B, E) calm2, (C, F) calm3. Note, genes we denote medaka calm1, calm2 and calm3 have previously been denoted CaM-A, CaM-B and CaM-C, but we have re-named them due to the orthology relationships identified by our phylogenetic analysis. Relative expression values are scaled so that expression in the lower jaw of embryos = 1. Standard error is indicated. Two-way ANOVAs show a statistically significant difference in expression for calm1 in halfbeak (P < 0.001), but not medaka (P > 0.1). Neither calm2 nor calm3 show differential expression for halfbeak or medaka (P > 0.1) (see Table 1). RQ = relative quantitation.
Mentions: The molecular basis of heterochronic growth was examined in halfbeak as a first step to determining the molecular basis of craniofacial diversity within the Belonoidei. The expression of candidate genes, including bmp2, bmp4, runx2, sox9b and three calmodulin orthologues, denoted calm1, calm2 and calm3 was compared between upper and lower jaws at a range of developmental stages that appear to be important for jaw outgrowth (Figure 5A, Additional file6: Figure S4, Additional file3: Table S2). We observed significantly differential expression for four of the seven genes examined, based on two-way ANOVAs (Table 1). The majority of genes in our study were upregulated in the lower jaw relative to the upper jaw - amongst these were sox9b, runx2 and calm1, while bmp2 was upregulated in the upper jaw (Figure 5B-D, Figure 6D). As both sox9b and runx2 were upregulated in the lower jaw, we infer that both chondrogenic (cartilage-forming) and osteogenic (bone-forming) pathways are required for the outgrowth of the lower jaw, presumably the result of their enhanced expression in Meckel’s cartilages and the dentaries respectively (Additional file3: Table S2). Expression of bmp2 was significantly higher in the upper jaw, which matches neither runx2 nor sox9b (Figure 5B-D), reducing the possibility that it is involved in either bone or cartilage development for the stages we examined.

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.