Eye size does not change with artificial selection on relative telencephalon size in guppies (Poecilia reticulata).

INTRODUCTION: Variation in eye size is sometimes closely associated with brain morphology. Visual information, detected by the retina, is transferred to the optic tectum to coordinate eye and body movements towards stimuli, and thereafter distributed into other brain regions for further processing. The telencephalon is an important visual processing region in many vertebrate species and a highly developed region in visually dependent species. Yet, the existence of a coevolutionary relationship between telencephalon size and eye size remains relatively unknown. METHODS: Here, we use male and female guppies artificially selected for small- and large-relative-telencephalon-size to test if artificial selection on telencephalon size results in changes in eye size. In addition, we performed an optomotor test as a proxy for visual acuity. RESULTS: We found no evidence that eye size changes with artificial selection on telencephalon size. Eye size was similar in both absolute and relative terms between the two selection regimes, but was larger in females. This is most likely because of the larger body size in females, but it could also reflect their greater need for visual capacity due to sex-specific differences in foraging and mating behaviour. Although the optomotor response was stronger in guppies with a larger telencephalon, we found no evidence for differences in visual acuity between the selection regimes. CONCLUSION: Our study suggests that eye size and visual perception in guppies does not change rapidly with strong artificial selection on telencephalon size.

Brain size does not predict learning strategies in a serial reversal learning test.

Reversal learning assays are commonly used across a wide range of taxa to investigate associative learning and behavioural flexibility. In serial reversal learning, the reward contingency in a binary discrimination is reversed multiple times. Performance during serial reversal learning varies greatly at the interspecific level, as some animals adopt a rule-based strategy that enables them to switch quickly between reward contingencies. A larger relative brain size, generating enhanced learning ability and increased behavioural flexibility, has been proposed to be an important factor underlying this variation. Here, we experimentally tested this hypothesis at the intraspecific level. We used guppies (Poecilia reticulata) artificially selected for small and large relative brain size, with matching differences in neuron number, in a serial reversal learning assay. We tested 96 individuals over 10 serial reversals and found that learning performance and memory were predicted by brain size, whereas differences in efficient learning strategies were not. We conclude that variation in brain size and neuron number is important for variation in learning performance and memory, but these differences are not great enough to cause the larger differences in efficient learning strategies observed at higher taxonomic levels.

Artificial selection for schooling behaviour and its effects on associative learning abilities.

The evolution of collective behaviour has been proposed to have important effects on individual cognitive abilities. Yet, in what way they are related remains enigmatic. In this context, the 'distributed cognition' hypothesis suggests that reliance on other group members relaxes selection for individual cognitive abilities. Here, we tested how cognitive processes respond to evolutionary changes in collective motion using replicate lines of guppies (Poecilia reticulata) artificially selected for the degree of schooling behaviour (group polarization) with >15% difference in schooling propensity. We assessed associative learning in females of these selection lines in a series of cognitive assays: colour associative learning, reversal learning, social associative learning, and individual and collective spatial associative learning. We found that control females were faster than polarization-selected females at fulfilling a learning criterion only in the colour associative learning assay, but they were also less likely to reach a learning criterion in the individual spatial associative learning assay. Hence, although testing several cognitive domains, we found weak support for the distributed cognition hypothesis. We propose that any cognitive implications of selection for collective behaviour lie outside of the cognitive abilities included in food-motivated associative learning for visual and spatial cues.

Sexual selection and the evolution of sperm morphology in sharks.

Post-copulatory sexual selection, and sperm competition in particular, is a powerful selective force shaping the evolution of sperm morphology. Although mounting evidence suggests that post-copulatory sexual selection influences the evolution of sperm morphology among species, recent evidence also suggests that sperm competition influences variation in sperm morphology at the intraspecific level. However, contradictory empirical results and limited taxonomic scope have led to difficulty in assessing the generality of sperm morphological responses to variation in the strength of sperm competition. Here, we use phylogenetically controlled analyses to explore the effects of sperm competition on sperm morphology and variance in sharks, a basal vertebrate group characterized by wide variation in rates of multiple mating by females, and consequently sperm competition risk. Our analyses reveal that shark species experiencing greater levels of sperm competition produce sperm with longer flagella and that sperm flagellum length is less variable in species under higher sperm competition risk. In contrast, neither the length of the sperm head and midpiece nor variation in sperm head and midpiece length was associated with sperm competition risk. Our findings demonstrate that selection influences both the inter- and intraspecific variation in sperm morphology and suggest that the flagellum is an important target of sexual selection in sharks. These findings provide important insight into patterns of selection on the ejaculate in a basal vertebrate lineage.

Plastic changes in brain morphology in relation to learning and environmental enrichment in the guppy (Poecilia reticulata).

Despite the common assumption that the brain is malleable to surrounding conditions mainly during ontogeny, plastic neural changes can occur also in adulthood. One of the driving forces responsible for alterations in brain morphology is increasing environmental complexity that may demand enhanced cognitive abilities (e.g. attention, memory and learning). However, studies looking at the relationship between brain morphology and learning are scarce. Here, we tested the effects of both learning and environmental enrichment on neural plasticity in guppies (Poecilia reticulata), by means of either a reversal-learning test or a spatial-learning test. Given considerable evidence supporting environmentally induced plastic alterations, two separate control groups that were not subjected to any cognitive test were included to account for potential changes induced by the experimental setup alone. We did not find any effect of learning on any of our brain measurements. However, we found strong evidence for an environmental effect, where fish given access to the spatial-learning environment had larger relative brain size and optic tectum size in relation to those exposed to the reversal-learning environment. Our results demonstrate the plasticity of the adult brain to respond adaptively mainly to environmental conditions, providing support for the environmental enhancement theory.

Brain size affects performance in a reversal-learning test.

It has become increasingly clear that a larger brain can confer cognitive benefits. Yet not all of the numerous aspects of cognition seem to be affected by brain size. Recent evidence suggests that some more basic forms of cognition, for instance colour vision, are not influenced by brain size. We therefore hypothesize that a larger brain is especially beneficial for distinct and gradually more complex aspects of cognition. To test this hypothesis, we assessed the performance of brain size selected female guppies (Poecilia reticulata) in two distinct aspects of cognition that differ in cognitive complexity. In a standard reversal-learning test we first investigated basic learning ability with a colour discrimination test, then reversed the reward contingency to specifically test for cognitive flexibility. We found that large-brained females outperformed small-brained females in the reversed-learning part of the test but not in the colour discrimination part of the test. Large-brained individuals are hence cognitively more flexible, which probably yields fitness benefits, as they may adapt more quickly to social and/or ecological cognitive challenges. Our results also suggest that a larger brain becomes especially advantageous with increasing cognitive complexity. These findings corroborate the significance of brain size for cognitive evolution.

Relative telencephalon size does not affect collective motion in the guppy (Poecilia reticulata).

Collective motion is common across all animal taxa, from swarming insects to schools of fish. The collective motion requires intricate behavioral integration among individuals, yet little is known about how evolutionary changes in brain morphology influence the ability for individuals to coordinate behavior in groups. In this study, we utilized guppies that were selectively bred for relative telencephalon size, an aspect of brain morphology that is normally associated with advanced cognitive functions, to examine its role in collective motion using an open-field assay. We analyzed high-resolution tracking data of same-sex shoals consisting of 8 individuals to assess different aspects of collective motion, such as alignment, attraction to nearby shoal members, and swimming speed. Our findings indicate that variation in collective motion in guppy shoals might not be strongly affected by variation in relative telencephalon size. Our study suggests that group dynamics in collectively moving animals are likely not driven by advanced cognitive functions but rather by fundamental cognitive processes stemming from relatively simple rules among neighboring individuals.

The link between relative brain size and cognitive ageing in female guppies (Poecilia reticulata) artificially selected for variation in brain size.

Cognitive ageing is the general process when certain mental skills gradually deteriorate with age. Across species, there is a pattern of a slower brain structure degradation rate in large-brained species. Hence, having a larger brain might buffer the impact of cognitive ageing and positively affect survival at older age. However, few studies have investigated the link between relative brain size and cognitive ageing at the intraspecific level. In particular, experimental data on how brain size affects brain function also into higher age is largely missing. We used 288 female guppies (Poecilia reticulata), artificially selected for large and small relative brain size, to investigate variation in colour discrimination and behavioural flexibility, at 4-6, 12 and 24 months of age. These ages are particularly interesting since they cover the life span from sexual maturation until maximal life length under natural conditions. We found no evidence for a slower cognitive ageing rate in large-brained females in neither initial colour discrimination nor reversal learning. Behavioural flexibility was predicted by large relative brain size in the youngest group, but the effect of brain size disappeared with increasing age. This result suggests that cognitive ageing rate is faster in large-brained female guppies, potentially due to the faster ageing and shorter lifespan in the large-brained selection lines. It also means that cognition levels align across different brain sizes with older age. We conclude that there are cognitive consequences of ageing that vary with relative brain size in advanced learning abilities, whereas fundamental aspects of learning can be maintained throughout the ecologically relevant life span.