Experience and motivation shape leader-follower interactions in fish shoals

Leadership is an important process shaping collective movement in some species. Recent work has demonstrated that experienced or motivated individuals can emerge as leaders, and provides insight into the mechanisms by which this occurs. Ultimately, leadership depends upon the effectiveness with which would-be leaders can entrain followers, and while the properties of leaders have received much attention, less is known about the factors that affect the propensity of their groupmates to follow them. Here the roles of experience and state (hunger) in shaping leader and follower behavior were investigated using shoals of sticklebacks (Gasterosteus aculeatus). A first experiment revealed that individuals trained to approach a target could entrain and lead their naïve groupmates out of a refuge towards it, and that they did so more effectively when they (the trained fish) were food-deprived. In the second experiment the hunger level of the trained fish was held constant, while that of the naïve fish was varied. Here, leadership by trained fish was only apparent when the hunger levels of the naïve group members were intermediate. When naïve fish were recently fed they took a long time to visit the target and their arrival times were not affected by the presence of a trained individual. Very hungry groups recruited to the target most rapidly, but again with no evidence of influence by their trained groupmates. These experiments demonstrate that leadership in animal groups depends not only upon the state and experience of the leader but also upon that of the potential followers.PostprintPeer reviewe

Space-use and sociability are not related to public-information use in ninespine sticklebacks

There has been much recent interest in both public information use, and the evolutionary origins and ecological consequences of animal personalities but surprisingly little integration of these two fields. Personality traits may impact upon the extent to which individuals respond to public information in a number of different ways. As a first step towards addressing some of these questions, in this study, we asked whether personality traits predicted public information use in ninespine sticklebacks (Pungitius pungitius). Over a 33-day period, subjects were scored twice for a number of behavioural traits, including measures of activity, exploration and shoaling tendency, and were exposed multiple times to a public information use foraging task, in which they were required to select the richer of two prey patches based upon the foraging success of two demonstrator groups. The repeatable (r=0.38–0.58) behavioural traits were reduced to two principle components describing space use and sociability. Neither of these was found to be related to either of two measures of public information use. While the personality traits that we considered did not co-vary with public information use in this species, they may well indirectly affect opportunity for exposure to public information, and this is an obvious avenue for further research.PostprintPeer reviewe

Sticklebacks show consistent prey-share hierarchies within but not between patchy and sequential prey distributions

This work was supported by the School of Biology’s Experimental Research Project (BL4201) program, (module BL4201: Experimental Research Project) at the University of St Andrews, UK.When animals compete, hierarchies can emerge. If the outcome of competition under different conditions is dependent upon different sets of attributes, then we may expect to see hierarchies that are domain-specific, rather than domain general. We tested this idea by comparing prey share hierarchies within shoals of sticklebacks Gasterosteus aculeatus as they foraged for patchily-distributed or for drifting prey. We found that prey share was correlated across pairs of patch- and pairs of drift-foraging trials, but not between the two conditions, suggesting that separate repeatable but independent prey share hierarchies arise for each for each type of prey distribution. We discuss possible underlying mechanisms and ecological implications of this finding.PostprintPeer reviewe

Social information use and social learning in non-grouping fishes

Funding: NERC (NE/D010365/1) and European Research Council advanced grants (EVOCULTURE 232823).Although it is natural to expect that group-living animals will utilize social learning, the expectation for non-grouping species is less clear. Only a few studies have explored the relationship between sociality and social learning. Here we presented 4 non-grouping fish species, fifteenspine sticklebacks (Spinachia spinachia), bullhead sculpins (Cottus gobio), stone loach (Barbatula barbatula) and juvenile European flounders (Platichthys flesus) with social information provided by groups of a shoal-forming heterospecific, the threespine stickleback (Gasterosteus aculeatus). Using a binary choice procedure we allowed individual test subjects to select between simulated prey patches. Although the test subjects could not sample the patches directly they were able to use information generated by the heterospecific demonstrators to select the “richer” of the 2 patches. For comparison we also recorded social information use in 2 shoaling species, threespine, and ninespine sticklebacks (Pungitius pungitius). We saw evidence of social information use and social learning in all 6 species, with no differences seen between social and non-grouping species. We argue that social learning is not likely to be restricted to group-living species, since many solitary species too are regularly exposed to social stimuli from both conspecifics and heterospecifics, and can benefit from using social information. We suggest that researchers have much to learn about the sensory, perceptive, and cognitive mechanisms underlying social learning, and the extent to which these vary (if at all) between grouping and non-grouping species.PostprintPeer reviewe

Experience shapes social information use in foraging fish

Funding: This work was funded by the Natural Environment Research Council (NE/D010365/1) to K.N.L.Many species of animal use social information, and in a variety of different contexts, but it is not clear to what degree their ability to do this depends upon their prior experience of the association between the behaviour of others and reward. We addressed this question in an experiment in which two stickleback species (Gasterosteus aculeatus and Pungitius pungitius) were exposed to a novel feeding task and then tested under a range of conditions. Using a fully-factorial training design, fish were either fed from the surface or the bottom of their tank, and at the same time were exposed to conspecifics feeding from the surface or bottom. At test, we showed that in order to be able to use demonstrator behaviour to anticipate the presence of food at the surface, test subjects needed first to have prior experience of both: sticklebacks responded to the behaviour of conspecifics that were feeding at the surface by rising higher in the water column themselves, but, crucially, they only did this if they had prior experience both of finding food at the water surface and of seeing others feed there. Moreover, they only displayed this response in the presence of feeding conspecifics, but not when the demonstrators were not feeding or were absent. The role of prior experience and learning in social information use is surprisingly understudied. We suggest that such work is vital if we are to understand the level at which natural selection operates in shaping social information use and social learning.PostprintPeer reviewe

Passive traps and sampling bias: social effects and personality affect trap-entry by sticklebacks

This research was funded by the University of St Andrews.Researchers routinely quantify the behaviour of subsets of animals, using their findings to make inferences about wider populations. Broader conclusions, however, may be inaccurate if the subjects that are tested are not representative of these populations. One way that this can arise is through sampling bias, which can occur if the method of collecting the test subjects disproportionately selects those with particular attributes, such that they end up being over‐ or under represented within the sample. Passive traps are associated with such sampling biases and have been shown to target certain behavioural phenotypes in a range of species. Here we asked whether funnel‐type fish traps were more likely to target more active and more social sticklebacks (Gasterosteus aculeatus). We found that more subjects entered the traps when they already contained conspecifics and that individual measures of activity predicted trap entry, with more active fish being captured sooner both when the traps already contained conspecifics and when they were empty. Unexpectedly, less‐social fish were captured sooner when the traps contained conspecifics. Sampling biases have the potential to skew the data collected by researchers and we therefore highlight the need to acknowledge and discuss potential for sampling biases and any consequences that may arise from this in published work. In the longer term, research that estimates the potential for sampling biases for various collection methods and species would be a valuable resource for helping to devise more representative sampling designs.Publisher PDFPeer reviewe

Morphological differences between habitats are associated with physiological and behavioural trade-offs in stickleback (Gasterosteus aculeatus)

F.S. and A.J.W.W. were supported by the Australian Research Council, M.M.W. was supported by The University of St Andrews and R.S.J. and J.T. were supported by Coventry UniversityLocal specialization can be advantageous for individuals and may increase the resilience of the species to environmental change. However, there may be trade-offs between morphological responses and physiological performance and behaviour. Our aim was to test whether habitat-specific morphology of stickleback (Gasterosteus aculeatus) interacts with physiological performance and behaviour at different salinities. We rejected the hypothesis that deeper body shape of fish from habitats with high predation pressure led to decreases in locomotor performance. However, there was a trade-off between deeper body shape and muscle quality. Muscle of deeper-bodied fish produced less force than that of shallow-bodied saltmarsh fish. Nonetheless, saltmarsh fish had lower swimming performance, presumably because of lower muscle mass overall coupled with smaller caudal peduncles and larger heads. Saltmarsh fish performed better in saline water (20 ppt) relative to freshwater and relative to fish from freshwater habitats. However, exposure to salinity affected shoaling behaviour of fish from all habitats and shoals moved faster and closer together compared with freshwater. We show that habitat modification can alter phenotypes of native species, but local morphological specialization is associated with trade-offs that may reduce its benefits.Publisher PDFPeer reviewe

Wave of mutilation : scavenging hermit crabs use social information to locate carcasses

Funding: Eastbio; Fisheries Society of the British Isles; St Andrews University Research Internship Scheme.Carcasses are patchily distributed and often short-lived resources, placing scavenging animals under pressure to locate them before they rot or are depleted by competitors. Scavengers may search for carcasses directly, or indirectly, using social information. Aggregations of feeding animals and their conspicuous competitive behaviour may be more readily detectable to searching scavengers than the carcass itself. Moreover, the actions of attendant scavengers upon the carcass, breaking it apart and releasing odour or chemical cues, may further enhance its detectability to others foraging nearby. Here we test this idea. In the first of two experiments performed in the field, we found that hermit crabs (Pagurus bernhardus) were attracted to shelled mussels (Mytilus edulis) that other hermit crabs were already feeding on. They showed no strong tendency to approach aggregations of conspecifics in the absence of food, nor conspecifics that were confined close to mussels but prevented from feeding on them. We speculated that through breaking up the carcass, the feeding hermit crabs released chemical cues and drifting particles of mussel tissue that further attracted other hermit crabs. We tested this in a second experiment, finding that finely chopped mussels attracted significantly more hermit crabs than did intact mussels. We suggest that scavenger feeding action upon carcasses makes these more detectable to others by releasing odour and particle plumes, a form of inadvertently produced social information.Peer reviewe

A four-questions perspective on public information use in sticklebacks (Gasterosteidae)

This research was supported by ERC Advanced (EVOCULTURE 232823) and NERC (NE/D010365/1) grants to KNL and grants from the NSF (IOS0744974, DEB1149160), NIH (R01GM115996), and Burroughs Wellcome Fund to MDS.Whether learning primarily reflects general processes or species-specific challenges is a long-standing matter of dispute. Here, we present a comprehensive analysis of public information use (PI-use) in sticklebacks (Gasterosteidae). PI-use is a form of social learning by which animals are able to assess the relative quality of resources, here prey patches, by observing the behaviour of others. PI-use was highly specific with only Pungitius and their closest relative Culaea inconstans showing evidence of PI-use. We saw no effects of ontogenetic experience upon PI-use in Pungitius pungitius. Experiments with live demonstrators and animated fish revealed that heightened activity and feeding strikes by foraging conspecifics are important cues in the transmission of PI. Finally, PI-use was the only form of learning in which P. pungitius and another stickleback, Gasterosteus aculeatus differed. PI-use in sticklebacks is species-specific and may represent an ‘ecological specialization’ for social foraging. Whether this reflects selection on perception, attentional or cognitive processes remains to be determined.Publisher PDFPeer reviewe

Mutations in REEP6 Cause Autosomal-Recessive Retinitis Pigmentosa

Retinitis pigmentosa (RP) is the most frequent form of inherited retinal dystrophy. RP is genetically heterogeneous and the genes identified to date encode proteins involved in a wide range of functional pathways, including photoreceptor development, phototransduction, the retinoid cycle, cilia, and outer segment development. Here we report the identification of biallelic mutations in Receptor Expression Enhancer Protein 6 (REEP6) in seven individuals with autosomal-recessive RP from five unrelated families. REEP6 is a member of the REEP/Yop1 family of proteins that influence the structure of the endoplasmic reticulum but is relatively unstudied. The six variants identified include three frameshift variants, two missense variants, and a genomic rearrangement that disrupts exon 1. Human 3D organoid optic cups were used to investigate REEP6 expression and confirmed the expression of a retina-specific isoform REEP6.1, which is specifically affected by one of the frameshift mutations. Expression of the two missense variants (c.383C>T [p.Pro128Leu] and c.404T>C [p.Leu135Pro]) and the REEP6.1 frameshift mutant in cultured cells suggest that these changes destabilize the protein. Furthermore, CRISPR-Cas9-mediated gene editing was used to produce Reep6 knock-in mice with the p.Leu135Pro RP-associated variant identified in one RP-affected individual. The homozygous knock-in mice mimic the clinical phenotypes of RP, including progressive photoreceptor degeneration and dysfunction of the rod photoreceptors. Therefore, our study implicates REEP6 in retinal homeostasis and highlights a pathway previously uncharacterized in retinal dystrophy