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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

Neuromasts and canal morphogenesis in Aulonocara stuartgranti and Tramitichromis sp. visualized with SEM. All SEM images are of late stage larvae and juveniles of Aulonocara, with the exception of C, which is of Tramitichromis. Arrows indicate presumptive CNs or position of CNs after canal enclosure; rostral to left in all images; see Figure 2 and 8 for definitions of St. 1 to St. 4. A) Infraorbital (IO), mandibular (MD) and preopercular (PO) presumptive CNs (canal neuromasts) in yolk sac larva (y, yolk; 7.5 mm SL). B) Close-up of A showing IO CNs at St. I, PO CNs at St. IIa. C)Tramitichromis sp. (7.5 mm SL): IO CNs at St. I, MD (MD1 to MD5) at St. I, and PO CNs at St. I or St. IIb. D) IO CNs at St. I and PO CNs at St. III/IV (11.5 mm; same individual as in Figure 6C,D). Other neuromasts are small SNs (superficial neuromasts) that remain on skin. E) Four supraorbital (SO) CNs; SO1 is medial to olfactory organ (ol) (6.0 mm SL). F) SO canal with SO1 at St. I, medial to naris (n), SO2 and SO3 at St. IIb; SO 4 and SO5 at St. III/IV; SNs visible between SO canals (sn; 9.5 mm SL). G) SO canal at St. III/IV, arrows indicate SO1 to SO3; two pores caudal to position of right and left SO3 CNs will fuse to form medial pore (mp) (10 mm SL). H) Mandibular CNs (MD1 to MD5) at St. IIa (7 mm SL). I) MD canal with MD1 at St. IIa, MD2 to 4 at St. IIb, and MD5 at St. IIa. First two PO CNs are at St. IIb and St. III/IV (11 mm SL). J) MD and PO canals enclosed (St. III/IV), arrows show MD1 to MD5 and first two PO CNs (12 mm SL). K) Close-up of left MD canal in I, showing MD1 at St. IIa, and MD2 and MD3 at St. IIb; small SNs (sn) are round in contrast to diamond-shaped canal neuromasts (11 mm SL). L) Close-up of diamond-shaped CN, MD1, showing location of sensory hair cells in sensory strip elongated parallel to physiological orientation of hair cells and canal axis (double-headed arrow; 10 mm SL).
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Figure 7: Neuromasts and canal morphogenesis in Aulonocara stuartgranti and Tramitichromis sp. visualized with SEM. All SEM images are of late stage larvae and juveniles of Aulonocara, with the exception of C, which is of Tramitichromis. Arrows indicate presumptive CNs or position of CNs after canal enclosure; rostral to left in all images; see Figure 2 and 8 for definitions of St. 1 to St. 4. A) Infraorbital (IO), mandibular (MD) and preopercular (PO) presumptive CNs (canal neuromasts) in yolk sac larva (y, yolk; 7.5 mm SL). B) Close-up of A showing IO CNs at St. I, PO CNs at St. IIa. C)Tramitichromis sp. (7.5 mm SL): IO CNs at St. I, MD (MD1 to MD5) at St. I, and PO CNs at St. I or St. IIb. D) IO CNs at St. I and PO CNs at St. III/IV (11.5 mm; same individual as in Figure 6C,D). Other neuromasts are small SNs (superficial neuromasts) that remain on skin. E) Four supraorbital (SO) CNs; SO1 is medial to olfactory organ (ol) (6.0 mm SL). F) SO canal with SO1 at St. I, medial to naris (n), SO2 and SO3 at St. IIb; SO 4 and SO5 at St. III/IV; SNs visible between SO canals (sn; 9.5 mm SL). G) SO canal at St. III/IV, arrows indicate SO1 to SO3; two pores caudal to position of right and left SO3 CNs will fuse to form medial pore (mp) (10 mm SL). H) Mandibular CNs (MD1 to MD5) at St. IIa (7 mm SL). I) MD canal with MD1 at St. IIa, MD2 to 4 at St. IIb, and MD5 at St. IIa. First two PO CNs are at St. IIb and St. III/IV (11 mm SL). J) MD and PO canals enclosed (St. III/IV), arrows show MD1 to MD5 and first two PO CNs (12 mm SL). K) Close-up of left MD canal in I, showing MD1 at St. IIa, and MD2 and MD3 at St. IIb; small SNs (sn) are round in contrast to diamond-shaped canal neuromasts (11 mm SL). L) Close-up of diamond-shaped CN, MD1, showing location of sensory hair cells in sensory strip elongated parallel to physiological orientation of hair cells and canal axis (double-headed arrow; 10 mm SL).

Mentions: Hatching occurred prior to 7 dpf in both Tramitichromis and Aulonocara. Yolk sac absorption started by 8 dpf and was complete by 20 to 22 dpf (at 10 to 11 mm SL), when young normally emerge from the mother’s mouth. Neuromasts were evident at hatch, and presumptive canal neuromasts (those that will become enclosed in the lateral line canals) then became distinct in size from superficial neuromasts that remain on the skin (Figures 6 and 7). Canal enclosure started at 8 and 11 mm SL (11 and 16 dpf) in the SO canal, and at 10 and 11 mm SL (23 and 19 dpf) in the MD canal in Tramitichromis and Aulonocara, respectively (Figure 7).


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

Bird NC, Webb JF - Evodevo (2014)

Neuromasts and canal morphogenesis in Aulonocara stuartgranti and Tramitichromis sp. visualized with SEM. All SEM images are of late stage larvae and juveniles of Aulonocara, with the exception of C, which is of Tramitichromis. Arrows indicate presumptive CNs or position of CNs after canal enclosure; rostral to left in all images; see Figure 2 and 8 for definitions of St. 1 to St. 4. A) Infraorbital (IO), mandibular (MD) and preopercular (PO) presumptive CNs (canal neuromasts) in yolk sac larva (y, yolk; 7.5 mm SL). B) Close-up of A showing IO CNs at St. I, PO CNs at St. IIa. C)Tramitichromis sp. (7.5 mm SL): IO CNs at St. I, MD (MD1 to MD5) at St. I, and PO CNs at St. I or St. IIb. D) IO CNs at St. I and PO CNs at St. III/IV (11.5 mm; same individual as in Figure 6C,D). Other neuromasts are small SNs (superficial neuromasts) that remain on skin. E) Four supraorbital (SO) CNs; SO1 is medial to olfactory organ (ol) (6.0 mm SL). F) SO canal with SO1 at St. I, medial to naris (n), SO2 and SO3 at St. IIb; SO 4 and SO5 at St. III/IV; SNs visible between SO canals (sn; 9.5 mm SL). G) SO canal at St. III/IV, arrows indicate SO1 to SO3; two pores caudal to position of right and left SO3 CNs will fuse to form medial pore (mp) (10 mm SL). H) Mandibular CNs (MD1 to MD5) at St. IIa (7 mm SL). I) MD canal with MD1 at St. IIa, MD2 to 4 at St. IIb, and MD5 at St. IIa. First two PO CNs are at St. IIb and St. III/IV (11 mm SL). J) MD and PO canals enclosed (St. III/IV), arrows show MD1 to MD5 and first two PO CNs (12 mm SL). K) Close-up of left MD canal in I, showing MD1 at St. IIa, and MD2 and MD3 at St. IIb; small SNs (sn) are round in contrast to diamond-shaped canal neuromasts (11 mm SL). L) Close-up of diamond-shaped CN, MD1, showing location of sensory hair cells in sensory strip elongated parallel to physiological orientation of hair cells and canal axis (double-headed arrow; 10 mm SL).
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4066827&req=5

Figure 7: Neuromasts and canal morphogenesis in Aulonocara stuartgranti and Tramitichromis sp. visualized with SEM. All SEM images are of late stage larvae and juveniles of Aulonocara, with the exception of C, which is of Tramitichromis. Arrows indicate presumptive CNs or position of CNs after canal enclosure; rostral to left in all images; see Figure 2 and 8 for definitions of St. 1 to St. 4. A) Infraorbital (IO), mandibular (MD) and preopercular (PO) presumptive CNs (canal neuromasts) in yolk sac larva (y, yolk; 7.5 mm SL). B) Close-up of A showing IO CNs at St. I, PO CNs at St. IIa. C)Tramitichromis sp. (7.5 mm SL): IO CNs at St. I, MD (MD1 to MD5) at St. I, and PO CNs at St. I or St. IIb. D) IO CNs at St. I and PO CNs at St. III/IV (11.5 mm; same individual as in Figure 6C,D). Other neuromasts are small SNs (superficial neuromasts) that remain on skin. E) Four supraorbital (SO) CNs; SO1 is medial to olfactory organ (ol) (6.0 mm SL). F) SO canal with SO1 at St. I, medial to naris (n), SO2 and SO3 at St. IIb; SO 4 and SO5 at St. III/IV; SNs visible between SO canals (sn; 9.5 mm SL). G) SO canal at St. III/IV, arrows indicate SO1 to SO3; two pores caudal to position of right and left SO3 CNs will fuse to form medial pore (mp) (10 mm SL). H) Mandibular CNs (MD1 to MD5) at St. IIa (7 mm SL). I) MD canal with MD1 at St. IIa, MD2 to 4 at St. IIb, and MD5 at St. IIa. First two PO CNs are at St. IIb and St. III/IV (11 mm SL). J) MD and PO canals enclosed (St. III/IV), arrows show MD1 to MD5 and first two PO CNs (12 mm SL). K) Close-up of left MD canal in I, showing MD1 at St. IIa, and MD2 and MD3 at St. IIb; small SNs (sn) are round in contrast to diamond-shaped canal neuromasts (11 mm SL). L) Close-up of diamond-shaped CN, MD1, showing location of sensory hair cells in sensory strip elongated parallel to physiological orientation of hair cells and canal axis (double-headed arrow; 10 mm SL).
Mentions: Hatching occurred prior to 7 dpf in both Tramitichromis and Aulonocara. Yolk sac absorption started by 8 dpf and was complete by 20 to 22 dpf (at 10 to 11 mm SL), when young normally emerge from the mother’s mouth. Neuromasts were evident at hatch, and presumptive canal neuromasts (those that will become enclosed in the lateral line canals) then became distinct in size from superficial neuromasts that remain on the skin (Figures 6 and 7). Canal enclosure started at 8 and 11 mm SL (11 and 16 dpf) in the SO canal, and at 10 and 11 mm SL (23 and 19 dpf) in the MD canal in Tramitichromis and Aulonocara, respectively (Figure 7).

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