Lateral lines, a major sensory modality in fishes, are diverse among taxa, but their intraspecific variation has received limited attention. We examined numbers of superficial neuromasts on the buttressing lateral plates (LP) of 1910 threespine stickleback (Gasterosteus aculeatus Linnaeus, 1758) from 26 ecologically and morphologically diverse populations on the Haida Gwaii archipelago, western Canada. Extending from previous studies, we predicted that (i) highly stained dystrophic localities would have threespine stickleback with elevated numbers of neuromasts per plate due to a greater reliance on non-visual sensory modalities and (ii) that LP count and neuromast numbers per plate would functionally covary with predatory assemblage. We found that there were no differences in neuromast count across major habitats (marine, lake, stream), but clear-water populations and those with predatory fish had significantly more neuromasts per plate than most populations in highly stained dystrophic lakes, the effects being accentuated on the first buttressing plate (LP4). We also report the first evidence that neuromast counts per plate are sexually dimorphic, with males having a greater density of neuromasts in most populations. Two transplant experiments between ecologically opposite habitats indicate that within 12 generations, neuromast counts per plate can rapidly shift in response to a change in habitat.

Threespine stickleback exhibit a row of superficial neuromasts that project through the bony plates on each side of the trunk and which constitute an important sensory modality for detection of near-field water motion. Previously, we have shown that numbers of neuromasts on each structural plate are highly variable among populations. In the current paper, we expand this study to evaluate the extent of deviation from bilateral symmetry of 4344 fish in 57 natural and three transplant populations of threespine stickleback from lakes, streams and oceanic habitats of coastal British Columbia, predicting that neuromasts would be largely bilaterally symmetrical for optimal detection of external stimuli. In contrast, we found asymmetry in all populations, the greatest amount occurring on the anterior buttressing lateral plates and on populations with the fewest neuromasts. We found no consistent trends of signed (directional) asymmetry (SA) among the populations while relative absolute asymmetry (RAA) is lower in dystrophic (stained) habitats than in clearwater habitats (p < 0.001), except for fish with few neuromasts. Sexual dimorphism in RAA is also greater in dystrophic habitats (p < 0.001). Transplants from stained lakes to unstained ponds resulted in a 0.1% to 14% difference in RAA from the source population in less than 12 generations but varied in direction among experiments. Our data suggest a widespread tendency for populations exposed to reduced photic information to exhibit reduced asymmetry in their lateral line system, which can change rapidly in response to a new environment.

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Behavioural asymmetry, typically referred to as laterality, is widespread among bilaterians and is often associated with asymmetry in brain structure. However, the influence of sensory receptor asymmetry on laterality has undergone limited investigation. Here we use threespine stickleback (Gasterosteus aculeatus) to investigate the influence of lateral line asymmetry on laterality during lab simulations of three mechanosensation-dependent behaviours: predator evasion, prey localization and rheotaxis. We recorded the response of stickleback to impacts at the water surface and water flow in photic conditions and low-frequency oscillations in the dark, across four repeat trials. We then compared individuals’ laterality to asymmetry in the number of neuromasts on either side of their body. Stickleback hovered with their right side against the arena wall 57% of the time (P&lt;0.001) in illuminated surface impact trials and 56% of the time in (P=0.085) dark low-frequency stimulation trials. Light regime modulated the effect of neuromast count on laterality, as fish with more neuromasts were more likely to hover with the wall on their right during illumination (P=0.007) but were less likely to do so in darkness (P=0.025). Population level laterality diminished in later trials across multiple behaviours and individuals did not show a consistent side bias in any behaviours. Our results demonstrate a complex relationship between sensory structure asymmetry and laterality, suggesting that laterality is modulated multiple sensory modalities and temporally dynamic.