Local adaptation can be a potent force in speciation, with environmental heterogeneity leading to niche specialization and population divergence. However, local adaption often requires nonrandom mating to generate reproductive isolation. Population divergence in sensory properties can be particularly consequential in speciation, affecting both ecological adaptation and sexual communication. Pundamilia pundamila and Pundamilia nyererei are two closely related African cichlid species that differ in male coloration, blue vs. red. They co-occur at rocky islands in southern Lake Victoria, but inhabit different depth ranges with different light environments. The species differ in colour vision properties, and females exert species-specific preferences for blue vs. red males. Here, we investigated the mechanistic link between colour vision and preference, which could provide a rapid route to reproductive isolation. We tested the behavioural components of this link by experimentally manipulating colour perception - we raised both species and their hybrids under light conditions mimicking shallow and deep habitats - and tested female preference for blue and red males under both conditions. We found that rearing light significantly affected female preference: shallow-reared females responded more strongly to P. pundamilia males and deep-reared females favoured P. nyererei males - implying that visual development causally affects mate choice. These results are consistent with sensory drive predictions, suggesting that the visual environment is key to behavioural isolation of these species. However, the observed plasticity could also make the species barrier vulnerable to environmental change: species-assortative preferences were weaker in females that were reared in the other species' light condition.

Trophically transmitted parasites frequently increase their hosts' risk-taking behaviour, to facilitate transmission to the next host. Whether such elevated risk-taking can spill over to uninfected group members is, however, unknown. To investigate this, we confronted groups of 6 three-spined sticklebacks, Gasterosteus aculeatus, containing 0, 2, 4 or 6 experimentally infected individuals with a simulated bird attack and studied their risk-taking behaviour. As a parasite, we used the tapeworm Schistocephalus solidus, which increases the risk-taking of infected sticklebacks, to facilitate transmission to its final host, most often piscivorous birds. Before the attack, infected and uninfected individuals did not differ in their risk-taking. However, after the attack, individuals in groups with only infected members showed lower escape responses and higher risk-taking than individuals from groups with only uninfected members. Importantly, uninfected individuals adjusted their risk-taking behaviour to the number of infected group members, taking more risk with an increasing number of infected group members. Infected individuals, however, did not adjust their risk-taking to the number of uninfected group members. Our results show that behavioural manipulation by parasites does not only affect the infected host, but also uninfected group members, shedding new light on the social dynamics involved in host–parasite interactions.

Many prey species have evolved collective responses to avoid predation. They rapidly transfer information about potential predators to trigger and coordinate escape waves. Predation avoidance behaviour is often manipulated by trophically transmitted parasites, to facilitate their transmission to the next host. We hypothesized that the presence of infected, behaviourally altered individuals might disturb the spread of escape waves. We used the tapeworm Schistocephalus solidus , which increases risk-taking behaviour and decreases social responsiveness of its host, the three-spined stickleback, to test this hypothesis. Three subgroups of sticklebacks were placed next to one another in separate compartments with shelter. The middle subgroup contained either uninfected or infected sticklebacks. We confronted an outer subgroup with an artificial bird strike and studied how the escape response spread through the subgroups. With uninfected sticklebacks in the middle, escape waves spread rapidly through the entire shoal and fish remained in shelter thereafter. With infected sticklebacks in the middle, the escape wave was disrupted and uninfected fish rarely used the shelter. Infected individuals can disrupt the transmission of flight responses, thereby not only increasing their own predation risk but also that of their uninfected shoal members. Our study uncovers a potentially far-reaching fitness consequence of grouping with infected individuals.

A key benefit of sociality is a reduction in predation risk. Cohesive group behaviour and rapid collective decision making are essential for reducing predation risk in groups. Parasite infection might reduce an individuals’ grouping behaviours and thereby change the behaviour of the group as a whole. To investigate the relationship between parasite infection and grouping behaviours, we studied groups of three-spined sticklebacks, Gasterosteus aculeatus, varying the number of individuals experimentally infected with the cestode Schistocephalus solidus. We studied groups of six sticklebacks containing 0, 2, 3, 4 or 6 infected individuals before and after a simulated bird attack. We predicted that infected individuals would have reduced shoaling and swimming speed and that the presence of infected individuals within a group would reduce group cohesion and speed. Uninfected fish increased shoaling and reduced swimming speed more than infected fish after the bird attack. In groups containing both infected and uninfected fish, the group behaviours were dominated by the more frequent character (uninfected versus infected). Interestingly, groups with equal numbers of uninfected and infected fish showed the least shoaling and had the lowest swimming speeds, suggesting that these groups failed to generate a majority and therefore displayed signs of indecisiveness by reducing their swimming speed the most. Our results provide evidence for a negative effect of infection on a group’s shoaling behaviour, thereby potentially deteriorating collective decision making. The presence of infected individuals might thus have far-reaching consequences in natural populations under predation risk. Significance statement Parasite-infected individuals often show deviating group behaviours. This might reduce the anti-predator benefits of group living. However, it is unknown whether such deviations in group behaviour might influence the shoaling behaviour of uninfected group members and thereby the behaviour of the group as a whole. By experimentally infecting sticklebacks and investigating groups varying in infection rates, we show that infected sticklebacks differ in their shoaling behaviours from uninfected sticklebacks. Additionally, the presence of infected sticklebacks within the group affected the behaviour of uninfected shoal members. We show that shoals of infected fish are less cohesive and move slower compared to shoals of uninfected fish. Furthermore, we show that the infection rate of the shoal is crucial for how the group behaves.