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Heterochrony, modularity, and the functional evolution of the mechanosensory lateral line canal system of fishes.

Bird NC, Webb JF - Evodevo (2014)

Bottom Line: A faster rate of increase in canal diameter and neuromast width (but not length), and a delay in onset of canal morphogenesis were found in Aulonocara relative to Tramitichromis.Thus, canal and neuromast morphology are more strongly influenced by their identities as features of the lateral line system than by the attributes of the dermatocranial bones in which the canals are found.Rate heterochrony manifested during the larval stage ensures that the widened canal phenotype, known to be associated with benthic prey detection in adult Aulonocara, is already present before feeding commences.

View Article: PubMed Central - HTML - PubMed

Affiliation: Current address: Department of Biological Sciences, University of Rhode Island, 120 Flagg Road, Kingston RI 02881, USA.

ABSTRACT

Background: The canals of the mechanosensory lateral line system are components of the dermatocranium, and demonstrate phenotypic variation in bony fishes. Widened lateral line canals evolved convergently in a limited number of families of teleost fishes and it had been hypothesized that they evolved from narrow canals via heterochrony and explore modularity in the lateral line system. Two species of cichlids with different canal phenotypes were used to test a hypothesis of heterochrony. Histological material prepared from ontogenetic series of Aulonocara stuartgranti (widened canals) and Tramitichromis sp. (narrow canals) was analyzed using ANCOVA to determine rates of increase in canal diameter and neuromast size (length, width) and to compare the timing of onset of critical stages in canal morphogenesis (enclosure, ossification).

Results: A faster rate of increase in canal diameter and neuromast width (but not length), and a delay in onset of canal morphogenesis were found in Aulonocara relative to Tramitichromis. However, rates of increase in canal diameter and neuromast size among canals, among canal portions and among canals segments reveal similar trends within both species.

Conclusion: The evolution of widened lateral line canals is the result of dissociated heterochrony - acceleration in the rate of increase of both canal diameter and neuromast size, and delay in the onset of canal morphogenesis, in Aulonocara (widened canals) relative to Tramitichromis (narrow canals). Common rates of increase in canal diameter and neuromast size among canal portions in different dermatocranial bones and among canal segments reflect the absence of local heterochronies, and suggest modular integration among canals in each species. Thus, canal and neuromast morphology are more strongly influenced by their identities as features of the lateral line system than by the attributes of the dermatocranial bones in which the canals are found. Rate heterochrony manifested during the larval stage ensures that the widened canal phenotype, known to be associated with benthic prey detection in adult Aulonocara, is already present before feeding commences. Heterochrony can likely explain the convergent evolution of widened lateral line canals among diverse taxa. The lateral line system provides a valuable context for novel analyses of the relationship between developmental processes and the evolution of behaviorally and ecologically relevant phenotypes in fishes.

No MeSH data available.


Related in: MedlinePlus

Ontogenetic trends in canal diameter and neuromast size (length, width) in SO and MD canals. A-C) Comparison of rates of increase in three variables: canal diameter (A), neuromast length (B) and neuromast width (C) in Tramitichromis. D-F) Comparison of rates of increase in three variables: canal diameter (D), neuromast length (E) and neuromast width (F) in Aulonocara derived from histological material. See Tables 2 and 4 for statistical analysis. P <0.05 = significant; N.S. = no significant difference in rate of increase in neuromast size between supraorbital (SO) and mandibular (MD) canals.
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Figure 11: Ontogenetic trends in canal diameter and neuromast size (length, width) in SO and MD canals. A-C) Comparison of rates of increase in three variables: canal diameter (A), neuromast length (B) and neuromast width (C) in Tramitichromis. D-F) Comparison of rates of increase in three variables: canal diameter (D), neuromast length (E) and neuromast width (F) in Aulonocara derived from histological material. See Tables 2 and 4 for statistical analysis. P <0.05 = significant; N.S. = no significant difference in rate of increase in neuromast size between supraorbital (SO) and mandibular (MD) canals.

Mentions: The analysis of developmental rates for canal diameter, neuromast length and neuromast width within each species at the level of canal, canal portion and canal segment revealed few rate differences that would indicate the presence of local heterochronies within species and thus modularity. Rates of increase in SO and MD canal diameter and neuromast size (length, width) were not statistically different between canals in either species (Tables 2 and 4, Figure 11). The two portions of the SO canal and the MD canal demonstrated similar rates of increase in canal diameter and neuromast size in each species (Additional file 1: Tables S3 and S8). In contrast, the analysis of developmental rates among SO and among MD canal segments revealed some variability, but consistent patterns could not be detected in either species (Additional file 1: Tables S7 and S9).


Heterochrony, modularity, and the functional evolution of the mechanosensory lateral line canal system of fishes.

Bird NC, Webb JF - Evodevo (2014)

Ontogenetic trends in canal diameter and neuromast size (length, width) in SO and MD canals. A-C) Comparison of rates of increase in three variables: canal diameter (A), neuromast length (B) and neuromast width (C) in Tramitichromis. D-F) Comparison of rates of increase in three variables: canal diameter (D), neuromast length (E) and neuromast width (F) in Aulonocara derived from histological material. See Tables 2 and 4 for statistical analysis. P <0.05 = significant; N.S. = no significant difference in rate of increase in neuromast size between supraorbital (SO) and mandibular (MD) canals.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4066827&req=5

Figure 11: Ontogenetic trends in canal diameter and neuromast size (length, width) in SO and MD canals. A-C) Comparison of rates of increase in three variables: canal diameter (A), neuromast length (B) and neuromast width (C) in Tramitichromis. D-F) Comparison of rates of increase in three variables: canal diameter (D), neuromast length (E) and neuromast width (F) in Aulonocara derived from histological material. See Tables 2 and 4 for statistical analysis. P <0.05 = significant; N.S. = no significant difference in rate of increase in neuromast size between supraorbital (SO) and mandibular (MD) canals.
Mentions: The analysis of developmental rates for canal diameter, neuromast length and neuromast width within each species at the level of canal, canal portion and canal segment revealed few rate differences that would indicate the presence of local heterochronies within species and thus modularity. Rates of increase in SO and MD canal diameter and neuromast size (length, width) were not statistically different between canals in either species (Tables 2 and 4, Figure 11). The two portions of the SO canal and the MD canal demonstrated similar rates of increase in canal diameter and neuromast size in each species (Additional file 1: Tables S3 and S8). In contrast, the analysis of developmental rates among SO and among MD canal segments revealed some variability, but consistent patterns could not be detected in either species (Additional file 1: Tables S7 and S9).

Bottom Line: A faster rate of increase in canal diameter and neuromast width (but not length), and a delay in onset of canal morphogenesis were found in Aulonocara relative to Tramitichromis.Thus, canal and neuromast morphology are more strongly influenced by their identities as features of the lateral line system than by the attributes of the dermatocranial bones in which the canals are found.Rate heterochrony manifested during the larval stage ensures that the widened canal phenotype, known to be associated with benthic prey detection in adult Aulonocara, is already present before feeding commences.

View Article: PubMed Central - HTML - PubMed

Affiliation: Current address: Department of Biological Sciences, University of Rhode Island, 120 Flagg Road, Kingston RI 02881, USA.

ABSTRACT

Background: The canals of the mechanosensory lateral line system are components of the dermatocranium, and demonstrate phenotypic variation in bony fishes. Widened lateral line canals evolved convergently in a limited number of families of teleost fishes and it had been hypothesized that they evolved from narrow canals via heterochrony and explore modularity in the lateral line system. Two species of cichlids with different canal phenotypes were used to test a hypothesis of heterochrony. Histological material prepared from ontogenetic series of Aulonocara stuartgranti (widened canals) and Tramitichromis sp. (narrow canals) was analyzed using ANCOVA to determine rates of increase in canal diameter and neuromast size (length, width) and to compare the timing of onset of critical stages in canal morphogenesis (enclosure, ossification).

Results: A faster rate of increase in canal diameter and neuromast width (but not length), and a delay in onset of canal morphogenesis were found in Aulonocara relative to Tramitichromis. However, rates of increase in canal diameter and neuromast size among canals, among canal portions and among canals segments reveal similar trends within both species.

Conclusion: The evolution of widened lateral line canals is the result of dissociated heterochrony - acceleration in the rate of increase of both canal diameter and neuromast size, and delay in the onset of canal morphogenesis, in Aulonocara (widened canals) relative to Tramitichromis (narrow canals). Common rates of increase in canal diameter and neuromast size among canal portions in different dermatocranial bones and among canal segments reflect the absence of local heterochronies, and suggest modular integration among canals in each species. Thus, canal and neuromast morphology are more strongly influenced by their identities as features of the lateral line system than by the attributes of the dermatocranial bones in which the canals are found. Rate heterochrony manifested during the larval stage ensures that the widened canal phenotype, known to be associated with benthic prey detection in adult Aulonocara, is already present before feeding commences. Heterochrony can likely explain the convergent evolution of widened lateral line canals among diverse taxa. The lateral line system provides a valuable context for novel analyses of the relationship between developmental processes and the evolution of behaviorally and ecologically relevant phenotypes in fishes.

No MeSH data available.


Related in: MedlinePlus