Asymmetry in the lateral line of threespine stickleback, Gasterosteus aculeatus: ecology, evolution and behaviour
Date
2021-05-18
Authors
Planidin, Nicholas
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Abstract
Behavioural asymmetry (laterality) is widespread among conspicuously bilaterally symmetrical organisms, playing a part in many aspects of life history from reproduction to feeding. Laterality is typically thought to occur due to morphological asymmetry within the brain, in which one hemisphere becomes specialized for a given task. However, the influence of sensory receptor asymmetry on the development of lateralized behaviour has undergone little investigation. The role of inconspicuous receptor asymmetry in behavioural laterality is particularly important, given the ubiquity of small deviations from symmetry.
Here I have investigated morphological asymmetry in the lateral line, a series of mechanoreceptors called neuromasts that comprise one of the major sensory modalities of fishes. I examined a subset of the lateral line of 3,987 threespine stickleback from 64 populations from coastal British Columbia, characterizing neuromast count and asymmetry among habitats. Furthermore, I scored 657 stickleback from four experimental transplant populations relocated from stained lakes to unstained ponds, to determine whether or not neuromast count or asymmetry changes in a novel habitat. Neuromast count did not differ between oceanic and freshwater stickleback, or between sympatric lake-stream pairs but did differ among clarity regimes, ranging from a complete lack of neuromasts to a doubling of neuromasts compared to oceanic stickleback. Loss of neuromasts was associated with reduced light transmission, lower pH and a lack of piscivorous fishes. Stickleback with more lateral plates developed more neuromasts and males bore more neuromasts than females. One transplant pond underwent a 70% increase in neuromast count within just a couple of generations, whereas the other three transplant populations underwent more gradual change, suggesting both phenotypically plastic and genetic mechanisms underlying difference in neuromast counts among populations.
Asymmetry was widespread among individuals, differing by up to seven neuromasts between the two sides on a single bony plate. However, no populations exhibited a strong directional bias. The degree of absolute asymmetry differed among clarity regimes, with stickleback in stained habitats having less asymmetry in their neuromasts counts. Asymmetry did not differ between oceanic and freshwater populations or sympatric lake-stream pairs. Males exhibited greater asymmetry than females, particularly in large-bodied populations. As with neuromast count, neuromast asymmetry quickly changed in some transplant populations and more gradually in others, increasing by up to 14% in just a couple of generations.
To assess the functional consequences of my geographic survey, I experimentally tested 40 stickleback for their response to a simulated predator, localization of vibrations in the dark and rheotaxis. I compared behaviour and laterality to neuromast count and asymmetry measured by fluorescent microscopy. Stickleback with fewer neuromasts were more likely to respond to simulated predator strikes, but other non-lateralized behaviours were independent of neuromast count. The strongest laterality I observed was the ‘hugging’ of the arena wall with the right side 57% of the time, with laterality being present in other behaviours, albeit weakly. While some behaviours correlated with lateral line asymmetry, there was no consistent association between lateralized behaviour and asymmetry in the lateral line.
I found that ecological factors such as predation landscape and photo-regime shape both mechanoreceptor count and asymmetry in the lateral line, with potential phenotypic plasticity in both traits. The lateral line’s role in response to a model predator and lateralized behaviour supports the influence of mechanosensory asymmetry in eco-evolutionary dynamics.
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Keywords
stickleback, lateral line, asymmetry, laterality, ecology, evolution, behaviour