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

Abstract

BackgroundThe 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).ResultsA 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.ConclusionThe 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.

The mechanosensory lateral line is used to assess opponents and mediate aggressive behaviors during territorial interactions in an African cichlid fish

“…The more turbulent environment of rivers creates hydrodynamic noise, and the narrow canal morphology and small pore diameter help reduce noise to better detect relevant signals (Klein and Bleckmann, 2015). The distribution of cranial neuromasts in A. burtoni is consistent with all previously examined African cichlids, independent of whether they possess widened or narrow canals Bird and Webb, 2014). We did not observe any major neuromast differences between males and females, or between social and reproductive states.…”

Asymmetric Facial Bone Fragmentation Mirrors Asymmetric Distribution of Cranial Neuromasts in Blind Mexican Cavefish

“…The distribution of cranial neuromasts on the head of fish and amphibians presents itself as a highly complex phenotype, likely subject to a variety of genetic and environmental influences [13,14]. Given this complexity, we sought to develop a tool that would enable us to compare the distributions of neuromasts on one side of the head against the other.…”

Experimental evidence of the role of heterochrony in evolution of the Mesoamerican cichlids pigment patterns

“…Over the last few decades, numerous groups have detailed genetic and developmental mechanisms underlying diversification of different morphological and behavioral traits in cichlids (Brawand et al, ; Burress, ; Elmer et al, ; Koblmüller, Albertson, Genner, Sefc, & Takahashi, ; Salzburger, ; Wagner, Harmon, & Seehausen, ). Among the defined mechanisms underlying evolutionary change, the alteration in developmental timing and rate, or heterochrony, has been a common means shared in different lineages (Bird & Webb, ; Escobar‐Camacho & Carleton, ; Le Pabic, Cooper, & Schilling, ; O'Quin, Smith, Sharma, & Carleton, ; Parsons, Taylor, Powder, & Albertson, ; Webb, Bird, Carter, & Dickson, ; Powder, Milch, Asselin, & Albertson, ).…”