Sensory trait variation contributes to biased dispersal of threespine stickleback in flowing water

Abstract

Gene flow is widely thought to homogenize spatially separate populations, eroding effects of divergent selection. The resulting theory of 'migration-selection balance' is predicated on a common assumption that all genotypes are equally prone to dispersal. If instead certain genotypes are disproportionately likely to disperse, then migration can actually promote population divergence. For example, previous work has shown that threespine stickleback (Gasterosteus aculeatus) differ in their propensity to move up- or downstream ('rheotactic response'), which may facilitate genetic divergence between adjoining lake and stream populations of stickleback. Here, we demonstrate that intraspecific variation in a sensory system (superficial neuromast lines) contributes to this variation in swimming behaviour in stickleback. First, we show that intact neuromasts are necessary for a typical rheotactic response. Next, we showed that there is heritable variation in the number of neuromasts and that stickleback with more neuromasts are more likely to move downstream. Variation in pectoral fin shape contributes to additional variation in rheotactic response. These results illustrate how within-population quantitative variation in sensory and locomotor traits can influence dispersal behaviour, thereby biasing dispersal between habitats and favouring population divergence.

Functional diversity of the lateral line system among populations of a native Australian freshwater fish

“…It is interesting to note that all studies to date have focused on neuromast abundance, while ignoring other aspects of morphology (e.g. neuromast arrangement and orientation) that may play a part (Jiang et al, 2017). It is important to recognise that it is unlikely that lateral line morphology is influenced by a single selective agent and it is more probable that combinations of environmental variables (including those that we did not evaluate) act on multiple traits.…”

“…The general lack of studies linking variation in lateral line morphology with behaviour makes it difficult to predict the functional outcome of our findings. Nonetheless, if the behaviour of individuals with ablated neuromasts can be used as a proxy for the behaviour of individuals with low neuromast abundance (Jiang et al, 2017), then we can predict, from previous studies, that low numbers of neuromasts are associated with reduced navigational ability (Flammang and Lauder, 2013) and a reduction in the response to water disturbances (Yoshizawa et al, 2010) relative to individuals with high numbers of neuromasts. We speculate here that the increased number of SNs in rainbowfish populations from open-water habitats thus facilitates navigation in an environment in which sensory information from nearby obstacles is limited.…”

“…Although few studies have linked variation in neuromast abundance with behaviour, a recent study by Jiang et al (2017) has revealed that neuromast number is correlated with the strength of the rheotactic response in sticklebacks. Specifically, sticklebacks with more neuromasts displayed a stronger negative rheotactic response (they were displaced downstream, spent more time swimming upstream and downstream, and spent less time orientated upstream) than those with fewer neuromasts (Jiang et al, 2017).…”

“…Although few studies have linked variation in neuromast abundance with behaviour, a recent study by Jiang et al (2017) has revealed that neuromast number is correlated with the strength of the rheotactic response in sticklebacks. Specifically, sticklebacks with more neuromasts displayed a stronger negative rheotactic response (they were displaced downstream, spent more time swimming upstream and downstream, and spent less time orientated upstream) than those with fewer neuromasts (Jiang et al, 2017). While it is known that SNs play a role in numerous other behaviours including prey capture (Carton and Montgomery, 2004;Montgomery et al, 2002), predator avoidance (Montgomery et al, 2002) and social communication (Butler and Maruska, 2016;Partridge and Pitcher, 1980), we are aware of no other studies (besides Jiang et al, 2017) that have correlated neuromast abundance with the expression of a particular behavioural trait.…”

“…For example, while it is clear that the lateral line is used by larval zebrafish to respond to suction-feeding predators (McHenry et al, 2009), only one study has shown that exposure to environmental cues, such as predation risk, can affect the development of the lateral line system in fishes (Fischer et al, 2013). Interestingly, it has recently been revealed that variation in an individual's lateral line morphology can determine the intensity of the rheotactic response (Jiang et al, 2017). Nonetheless, with the exception of the abovementioned studies, we understand surprisingly little about the relationship between lateral line diversity and the ecology and behaviour of fishes.…”