Predation impacts brain allometry in female guppies (Poecilia reticulata).

Cognitive and sensory abilities are vital in affecting survival under predation risk, leading to selection on brain anatomy. However, how exactly predation and brain evolution are linked has not yet been resolved, as current empirical evidence is inconclusive. This may be due to predation pressure having different effects across life stages and/or due to confounding factors in ecological comparisons of predation pressure. Here, we used adult guppies (Poecilia reticulata) to experimentally test how direct predation during adulthood would impact the relative brain size and brain anatomy of surviving individuals to examine if predators selectively remove individuals with specific brain morphology. To this end, we compared fish surviving predation to control fish, which were exposed to visual and olfactory predator cues but could not be predated on. We found that predation impacted the relative size of female brains. However, this effect was dependent on body size, as larger female survivors showed relatively larger brains, while smaller survivors showed relatively smaller brains when compared to control females. We found no differences in male relative brain size between survivors and controls, nor for any specific relative brain region sizes for either sex. Our results corroborate the important, yet complex, role of predation as an important driver of variation in brain size.

Jumping out of trouble: evidence for a cognitive map in guppies (Poecilia reticulata).

Spatial cognitive abilities allow individuals to remember the location of resources such as food patches, predator hide-outs, or shelters. Animals typically incorporate learned spatial information or use external environmental cues to navigate their surroundings. A spectacular example of how some fishes move is through aerial jumping. For instance, fish that are trapped within isolated pools, cut off from the main body of water during dry periods, may jump over obstacles and direct their jumps to return to safe locations. However, what information such re-orientation behavior during jumping is based on remains enigmatic. Here we combine a lab and field experiment to test if guppies (Poecilia reticulata) incorporate learned spatial information and external environmental cues (visual and auditory) to determine where to jump. In a spatial memory assay we found that guppies were more likely to jump towards deeper areas, hence incorporating past spatial information to jump to safety. In a matched versus mismatched spatial cue experiment in the field, we found that animals only showed directed jumping when visual and auditory cues matched. We show that in unfamiliar entrapments guppies direct their jumps by combining visual and auditory cues, whereas in familiar entrapments they use a cognitive map. We hence conclude that jumping behavior is a goal-directed behavior, guided by different sources of information and involving important spatial cognitive skills.

The effect of experimental hybridization on cognition and brain anatomy: Limited phenotypic variation and transgression in Poeciliidae.

Hybridization can promote phenotypic variation and often produces trait combinations distinct from the parental species. This increase in available variation can lead to the manifestation of functional novelty when new phenotypes bear adaptive value under the environmental conditions in which they occur. Although the role of hybridization as a driver of variation and novelty in traits linked to fitness is well recognized, it remains largely unknown whether hybridization can fuel behavioral novelty by promoting phenotypic variation in brain morphology and/or cognitive traits. To address this question, we investigated the effect of hybridization on brain anatomy, learning ability, and cognitive flexibility in first- and second-generation hybrids of two closely related fish species (Poecilia reticulata and Poecilia wingei). Overall, we found that F1 and F2 hybrids showed intermediate brain morphology and cognitive traits compared to parental groups. Moreover, as phenotypic dispersion and transgression were low for both brain and cognitive traits, we suggest that hybridization is not a strong driver of brain anatomical and cognitive diversification in these Poeciliidae. To determine the generality of this conclusion, hybridization experiments with cognitive tests need to be repeated in other families.

Hybridization May Promote Variation in Cognitive Phenotypes in Experimental Guppy Hybrids.

AbstractHybridization is an important mechanism of evolution. While hybrids often express inferior traits and are selected against, hybridization can promote phenotypic variation and produce trait combinations distinct from the parentals, generating novel adaptive potential. Among other traits, hybridization can impact behavior and cognition and may reinforce species boundaries when hybrids show decreased cognitive abilities. However, the hypothesized role of hybridization in the diversification of cognitive phenotypes remains enigmatic. To test this idea, we compare the performance of female guppies (Poecilia reticulata), Endler's guppies (Poecilia wingei), and their experimental hybrids in color association and reversal learning. In addition, we introduce a new approach to compare multidimensional cognitive phenotypes. We found that hybrids showed intermediate learning abilities in both tasks compared with the parentals. Moreover, hybrids had slightly higher phenotypic dispersion, new trait combinations occurred in some hybrid individuals, and the mean phenotype of one hybrid group deviated away from the axis of variation of the parentals. Our method should hence be useful in further exploring how hybridization and other evolutionary processes impact behavioral and cognitive traits. Our results suggest that hybridization may promote cognitive variation and generate new trait combinations, even when learning performance at the group level is intermediate between parentals.

Residency and movement patterns of adult Port Jackson sharks (Heterodontus portusjacksoni) at a breeding aggregation site.

Examining the movement ecology of mesopredators is fundamental to developing an understanding of their biology, ecology and behaviour, as well as the communities and ecosystems they influence. The limited research on the residency and movements of benthic marine mesopredators has primarily used visual tags, which do not allow for the efficient and accurate monitoring of individual space use. In this study, the authors investigated the residency and movement patterns of Port Jackson sharks Heterodontus portusjacksoni (Meyer 1793) at a breeding aggregation site in Jervis Bay, south-eastern Australia, using passive acoustic telemetry to further our understanding of the movement ecology of these important mesopredators. Between 2012 and 2014, individuals were tagged with acoustic transmitters, and their residency and movements within the bay were monitored for up to 4 years. H. portusjacksoni showed strong preferences for particular reefs within and between breeding seasons. Males had significantly higher residency indices at their favoured sites relative to females, suggesting that males may be engaging in territorial behaviour. Conversely, female H. portusjacksoni exhibited higher roaming indices relative to males indicating that females may move between sites to assess males. Finally, H. portusjacksoni showed temporal variation in movements between reefs with individuals typically visiting more reefs at night relative to the day, dusk and dawn corresponding with their nocturnal habits.

Correction to: Effects of reward magnitude and training frequency on the learning rates and memory retention of the Port Jackson shark Heterodontus portusjacksoni.

In the original publication of the article, the Fig. 4 was erroneously published.

Effects of reward magnitude and training frequency on the learning rates and memory retention of the Port Jackson shark Heterodontus portusjacksoni.

The development of adaptive responses to novel situations via learning has been demonstrated in a wide variety of animal taxa. However, knowledge on the learning abilities of one of the oldest extant vertebrate groups, Chondrichthyes, remains limited. With the increasing interest in global wildlife tourism and shark feeding operations, it is important to understand the capacities of these animals to form associations between human activities and food. We used an operant conditioning regime with a simple spatial cognitive task to investigate the effects of reinforcement frequency and reward magnitude on the learning performance and memory retention of Port Jackson sharks (Heterodontus portusjacksoni). Twenty-four Port Jackson sharks were assigned one of four treatments differing in reward magnitude and reinforcement frequency (large magnitude-high frequency; large magnitude-low frequency; small magnitude-high frequency; small magnitude-low frequency). The sharks were trained over a 21-day period to compare the number of days that it took to learn to pass an assigned door to feed. Sharks trained at a high reinforcement frequency demonstrated faster learning rates and a higher number of passes through the correct door at the end of the trials, while reward magnitude had limited effects on learning rate. This suggests that a reduction in reinforcement frequency during tourism-related feeding operations is likely to be more effective in reducing the risk of sharks making associations with food than limiting the amount of food provided.

Lack of social preference between unfamiliar and familiar juvenile Port Jackson sharks Heterodontus portusjacksoni.

This study investigated whether captive-reared juvenile Port Jackson sharks Heterodontus portusjacksoni choose to aggregate and if familiarity is one of the mechanisms driving social preference. In a controlled binary-choice experiment, juvenile sharks were given the option to associate or not with unfamiliar conspecifics, or to associate or not with familiar conspecifics. In neither group did juvenile H. portusjacksoni actively choose to associate with conspecifics, but familiarity decreased the proportion of time spent near a conspecific only during the initial phase of the experiment. Treatment (1 or 3 shoal mates), sex and size had no effect on aggregation behaviour. These findings suggest that familiarity is not a driver of social preferences in juvenile H. portusjacksoni, contrary to results in another shark species. Additionally, adult H. portusjacksoni form large aggregations during the breeding season and actively associate with familiar sex and size-matched individuals, thus our results suggest the species undergoes an ontogenetic shift in social behaviour.

Food approach conditioning and discrimination learning using sound cues in benthic sharks.

The marine environment is filled with biotic and abiotic sounds. Some of these sounds predict important events that influence fitness while others are unimportant. Individuals can learn specific sound cues and 'soundscapes' and use them for vital activities such as foraging, predator avoidance, communication and orientation. Most research with sounds in elasmobranchs has focused on hearing thresholds and attractiveness to sound sources, but very little is known about their abilities to learn about sounds, especially in benthic species. Here we investigated if juvenile Port Jackson sharks could learn to associate a musical stimulus with a food reward, discriminate between two distinct musical stimuli, and whether individual personality traits were linked to cognitive performance. Five out of eight sharks were successfully conditioned to associate a jazz song with a food reward delivered in a specific corner of the tank. We observed repeatable individual differences in activity and boldness in all eight sharks, but these personality traits were not linked to the learning performance assays we examined. These sharks were later trained in a discrimination task, where they had to distinguish between the same jazz and a novel classical music song, and swim to opposite corners of the tank according to the stimulus played. The sharks' performance to the jazz stimulus declined to chance levels in the discrimination task. Interestingly, some sharks developed a strong side bias to the right, which in some cases was not the correct side for the jazz stimulus.

Laterality strength is linked to stress reactivity in Port Jackson sharks (Heterodontus portusjacksoni).

Cerebral lateralization is an evolutionarily deep-rooted trait, ubiquitous among the vertebrates and present even in some invertebrates. Despite the advantages of cerebral lateralization in enhancing cognition and facilitating greater social cohesion, large within population laterality variation exists in many animal species. It is proposed that this variation is maintained due links with inter-individual personality trait differences. Here we explored for lateralization in Port Jackson sharks (Heterodontus portusjacksoni) using T-maze turn and rotational swimming tasks. Additionally, we explored for a link between personality traits, boldness and stress reactivity, and cerebral lateralization. Sharks demonstrated large individual and sex biased laterality variation, with females demonstrating greater lateralization than males overall. Stress reactivity, but not boldness, was found to significantly correlate with lateralization strength. Stronger lateralized individuals were more reactive to stress. Demonstrating laterality in elasmobranchs for the first time indicates ancient evolutionary roots of vertebrate lateralization approximately 240 million years old. Greater lateralization in female elasmobranchs may be related enhancing females' ability to process multiple stimuli during mating, which could increase survivability and facilitate insemination. Despite contrasting evidence in teleost fishes, the results of this study suggest that stress reactivity, and other personality traits, may be linked to variation in lateralization.