Publications by authors named "Alexander Kotrschal"

50 Publications

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

Exp Gerontol 2021 Apr 26;146:111218. Epub 2020 Dec 26.

Department of Zoology, Stockholm University, Svante Arrhenius väg 18B, 10691 Stockholm, Sweden. Electronic address:

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.
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http://dx.doi.org/10.1016/j.exger.2020.111218DOI Listing
April 2021

Rapid evolution of coordinated and collective movement in response to artificial selection.

Sci Adv 2020 Dec 2;6(49). Epub 2020 Dec 2.

Department of Zoology/Ethology, Stockholm University, Stockholm, Sweden.

Collective motion occurs when individuals use social interaction rules to respond to the movements and positions of their neighbors. How readily these social decisions are shaped by selection remains unknown. Through artificial selection on fish (guppies, ) for increased group polarization, we demonstrate rapid evolution in how individuals use social interaction rules. Within only three generations, groups of polarization-selected females showed a 15% increase in polarization, coupled with increased cohesiveness, compared to fish from control lines. Although lines did not differ in their physical swimming ability or exploratory behavior, polarization-selected fish adopted faster speeds, particularly in social contexts, and showed stronger alignment and attraction responses to multiple neighbors. Our results reveal the social interaction rules that change when collective behavior evolves.
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http://dx.doi.org/10.1126/sciadv.aba3148DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7710366PMC
December 2020

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

J Exp Biol 2020 Dec 7;223(Pt 23). Epub 2020 Dec 7.

Department of Zoology, Stockholm University, Svante Arrhenius väg 18B, 10691, Stockholm, Sweden.

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 () 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.
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http://dx.doi.org/10.1242/jeb.235093DOI Listing
December 2020

Different mating contexts lead to extensive rewiring of female brain coexpression networks in the guppy.

Genes Brain Behav 2021 Mar 22;20(3):e12697. Epub 2020 Sep 22.

University of British Columbia, Department of Zoology and Biodiversity Research Centre, Vancouver, Canada.

Understanding the basis of behavior requires dissecting the complex waves of gene expression that underlie how the brain processes stimuli and produces an appropriate response. In order to determine the dynamic nature of the neurogenomic network underlying mate choice, we use transcriptome sequencing to capture the female neurogenomic response in two brain regions involved in sensory processing and decision-making under different mating and social contexts. We use differential coexpression (DC) analysis to evaluate how gene networks in the brain are rewired when a female evaluates attractive and nonattractive males, greatly extending current single-gene approaches to assess changes in the broader gene regulatory network. We find the brain experiences a remarkable amount of network rewiring in the different mating and social contexts we tested. Further analysis indicates the network differences across contexts are associated with behaviorally relevant functions and pathways, particularly learning, memory and other cognitive functions. Finally, we identify the loci that display social context-dependent connections, revealing the basis of how relevant neurological and metabolic pathways are differentially recruited in distinct social contexts. More broadly, our findings contribute to our understanding of the genetics of mating and social behavior by identifying gene drivers behind behavioral neural processes, illustrating the utility of DC analysis in neurosciences and behavior.
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http://dx.doi.org/10.1111/gbb.12697DOI Listing
March 2021

Relative Brain Size Is Predicted by the Intensity of Intrasexual Competition in Frogs.

Am Nat 2020 08 22;196(2):169-179. Epub 2020 Jun 22.

Competition over mates is a powerful force shaping trait evolution. For instance, better cognitive abilities may be beneficial in male-male competition and thus be selected for by intrasexual selection. Alternatively, investment in physical attributes favoring male performance in competition for mates may lower the resources available for brain development, and more intense male mate competition would coincide with smaller brains. To date, only indirect evidence for such relationships exists, and most studies are heavily biased toward primates and other homoeothermic vertebrates. We tested the association between male brain size (relative to body size) and male-male competition across species of Chinese anurans. Three indicators of the intensity of male mate competition-operational sex ratio (OSR), spawning-site density, and male forelimb muscle mass-were positively associated with relative brain size, whereas the absolute spawning group size was not. The relationship with the OSR and male forelimb muscle mass was stronger for the male than for the female brains. Taken together, our findings suggest that the increased cognitive abilities of larger brains are beneficial in male-male competition. This study adds taxonomic breadth to the mounting evidence for a prominent role of sexual selection in vertebrate brain evolution.
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http://dx.doi.org/10.1086/709465DOI Listing
August 2020

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

J Exp Biol 2020 08 4;223(Pt 15). Epub 2020 Aug 4.

Department of Zoology/Ethology, Stockholm University, Svante Arrhenius väg 18B, 10691 Stockholm, Sweden.

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 () 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.
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http://dx.doi.org/10.1242/jeb.224741DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7413604PMC
August 2020

Body mass variation is negatively associated with brain size: Evidence for the fat-brain trade-off in anurans.

Evolution 2020 07 27;74(7):1551-1557. Epub 2020 May 27.

Behavioural Ecology, Department of Animal Sciences, Wageningen University, Wageningen, The Netherlands.

Species can evolve diverse strategies to survive periods of uncertainty. Animals may either invest in energy storage, allowing them to decrease foraging costs, such as locomotion or risk of predation, or they may invest in better cognitive abilities helping them to flexibly adapt their behavior to meet novel challenges. Here, we test this idea of a fat-brain trade-off in 38 species of Chinese anurans by relating the coefficient of variation of body mass (CV ; as an indicator of how much animals invest into storage over the season) to brain anatomical features. After correcting for shared ancestry and body mass, we found a negative relationship between relative brain size and CV . This indicates that anurans seem to trade-off physiological and cognitive buffering during energy shortages. As similar patterns have been reported in arboreal mammals and primates our findings suggest that the fat-brain trade-off, where animals either invest into physiological or cognitive strategies to survive harsh conditions, may be a general pattern across vertebrates.
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http://dx.doi.org/10.1111/evo.13991DOI Listing
July 2020

Experimental translocations to low predation lead to non-parallel increases in relative brain size.

Biol Lett 2020 01 22;16(1):20190654. Epub 2020 Jan 22.

Department of Zoology/Ethology, Stockholm University, Svante Arrheniusväg 18B, 10691 Stockholm, Sweden.

Predation is a near ubiquitous factor of nature and a powerful selective force on prey. Moreover, it has recently emerged as an important driver in the evolution of brain anatomy, though population comparisons show ambiguous results with considerable unexplained variation. Here, we test the reproducibility of reduced predation on evolutionary trajectories of brain evolution. We make use of an introduction experiment, whereby guppies () from a single high predation stream were introduced to four low predation streams. After 8-9 years of natural selection in the wild and two generations of common garden conditions in the laboratory, we quantified brain anatomy. Relative brain region sizes did not differ between populations. However, we found a general increase and striking variation in relative brain size of introduced populations, which varied from no change to a 12.5% increase in relative brain weight, relative to the ancestral high predation population. We interpret this as evidence for non-parallel evolution, which implies a weak or inconsistent association of relative brain size with fitness in low predation sites. The evolution of brain anatomy appears sensitive to unknown environmental factors, or contingent on either chance events or historical legacies of environmental change.
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http://dx.doi.org/10.1098/rsbl.2019.0654DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7013489PMC
January 2020

Brain size affects responsiveness in mating behaviour to variation in predation pressure and sex ratio.

J Evol Biol 2020 02 7;33(2):165-177. Epub 2019 Nov 7.

Department of Zoology/Ethology, Stockholm University, Stockholm, Sweden.

Despite ongoing advances in sexual selection theory, the evolution of mating decisions remains enigmatic. Cognitive processes often require simultaneous processing of multiple sources of information from environmental and social cues. However, little experimental data exist on how cognitive ability affects such fitness-associated aspects of behaviour. Using advanced tracking techniques, we studied mating behaviours of guppies artificially selected for divergence in relative brain size, with known differences in cognitive ability, when predation threat and sex ratio was varied. In females, we found a general increase in copulation behaviour in when the sex ratio was female biased, but only large-brained females responded with greater willingness to copulate under a low predation threat. In males, we found that small-brained individuals courted more intensively and displayed more aggressive behaviours than large-brained individuals. However, there were no differences in female response to males with different brain size. These results provide further evidence of a role for female brain size in optimal decision-making in a mating context. In addition, our results indicate that brain size may affect mating display skill in male guppies. We suggest that it is important to consider the association between brain size, cognitive ability and sexual behaviour when studying how morphological and behavioural traits evolve in wild populations.
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http://dx.doi.org/10.1111/jeb.13556DOI Listing
February 2020

Yes, correct context is indeed the key: An answer to Haave-Audet et al. 2019.

J Evol Biol 2019 12 3;32(12):1450-1455. Epub 2019 Nov 3.

Department of Zoology, Stockholm University, Stockholm, Sweden.

We published a study recently testing the link between brain size and behavioural plasticity using brain size selected guppy (Poecilia reticulata) lines (2019, Journal of Evolutionary Biology, 32, 218-226). Only large-brained fish showed habituation to a new, but actually harmless environment perceived as risky, by increasing movement activity over the 20-day observation period. We concluded that "Our results suggest that brain size likely explains some of the variation in behavioural plasticity found at the intraspecific level". In a commentary published in the same journal, Haave-Audet et al. challenged the main message of our study, stating that (a) relative brain size is not a suitable proxy for cognitive ability and (b) habituation measured by us is likely not adaptive and costly. In our response, we first show that a decade's work has proven repeatedly that relative brain size is indeed positively linked to cognitive performance in our model system. Second, we discuss how switching from stressed to unstressed behaviour in stressful situations without real risk is likely adaptive. Finally, we point out that the main cost of behavioural plasticity in our case is the development and maintenance of the neural system needed for information processing, and not the expression of plasticity. We hope that our discussion with Haave-Audet et al. helps clarifying some central issues in this emerging research field.
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http://dx.doi.org/10.1111/jeb.13548DOI Listing
December 2019

Artificial selection on brain size leads to matching changes in overall number of neurons.

Evolution 2019 09 1;73(9):2003-2012. Epub 2019 Aug 1.

Department of Zoology, Faculty of Science, Charles University, 12844, Prague, Czech Republic.

Neurons are the basic computational units of the brain, but brain size is the predominant surrogate measure of brain functional capacity in comparative and cognitive neuroscience. This approach is based on the assumption that larger brains harbor higher numbers of neurons and their connections, and therefore have a higher information-processing capacity. However, recent studies have shown that brain mass may be less strongly correlated with neuron counts than previously thought. Till now, no experimental test has been conducted to examine the relationship between evolutionary changes in brain size and the number of brain neurons. Here, we provide such a test by comparing neuron number in artificial selection lines of female guppies (Poecilia reticulata) with >15% difference in relative brain mass and numerous previously demonstrated cognitive differences. Using the isotropic fractionator, we demonstrate that large-brained females have a higher overall number of neurons than small-brained females, but similar neuronal densities. Importantly, this difference holds also for the telencephalon, a key region for cognition. Our study provides the first direct experimental evidence that selection for brain mass leads to matching changes in number of neurons and shows that brain size evolution is intimately linked to the evolution of neuron number and cognition.
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http://dx.doi.org/10.1111/evo.13805DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6772110PMC
September 2019

Large brains, short life: selection on brain size impacts intrinsic lifespan.

Biol Lett 2019 05;15(5):20190137

Department of Zoology/Ethology, Stockholm University , Stockholm , Sweden.

The relationship between brain size and ageing is a paradox. The cognitive benefits of large brains should protect from extrinsic mortality and thus indirectly select for slower ageing. However, the substantial energetic cost of neural tissue may also impact the energetic budget of large-brained organisms, causing less investment in somatic maintenance and thereby faster ageing. While the positive association between brain size and survival in the wild is well established, no studies exist on the direct effects of brain size on ageing. Here we test how brain size influences intrinsic ageing in guppy ( Poecilia reticulata) brain size selection lines with 12% difference in relative brain size. Measuring survival under benign conditions, we find that large-brained animals live 22% shorter than small-brained animals and the effect is similar in both males and females. Our results suggest a trade-off between investment into brain size and somatic maintenance. This implies that the link between brain size and ageing is contingent on the mechanism of mortality, and selection for positive correlations between brain size and ageing should occur mainly under cognition-driven survival benefits from increased brain size. We show that accelerated ageing can be a cost of evolving a larger brain.
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http://dx.doi.org/10.1098/rsbl.2019.0137DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6548732PMC
May 2019

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

J Exp Biol 2019 05 21;222(Pt 10). Epub 2019 May 21.

Department of Zoology, Stockholm University, SE-106 91 Stockholm, Sweden.

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 (), 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.
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http://dx.doi.org/10.1242/jeb.200402DOI Listing
May 2019

Brain size predicts behavioural plasticity in guppies (Poecilia reticulata): An experiment.

J Evol Biol 2019 03 21;32(3):218-226. Epub 2018 Dec 21.

Department of Zoology, Stockholm University, Stockholm, Sweden.

Understanding how animal personality (consistent between-individual behavioural differences) arises has become a central topic in behavioural sciences. This endeavour is complicated by the fact that not only the mean behaviour of individuals (behavioural type) but also the strength of their reaction to environmental change (behavioural plasticity) varies consistently. Personality and cognitive abilities are linked, and we suggest that behavioural plasticity could also be explained by differences in brain size (a proxy for cognitive abilities), since accurate decisions are likely essential to make behavioural plasticity beneficial. We test this idea in guppies (Poecilia reticulata), artificially selected for large and small brain size, which show clear cognitive differences between selection lines. To test whether those lines differed in behavioural plasticity, we reared them in groups in structurally enriched environments and then placed adults individually into empty tanks, where we presented them daily with visual predator cues and monitored their behaviour for 20 days with video-aided motion tracking. We found that individuals differed consistently in activity and risk-taking, as well as in behavioural plasticity. In activity, only the large-brained lines demonstrated habituation (increased activity) to the new environment, whereas in risk-taking, we found sensitization (decreased risk-taking) in both brain size lines. We conclude that brain size, potentially via increasing cognitive abilities, may increase behavioural plasticity, which in turn can improve habituation to novel environments. However, the effects seem to be behaviour-specific. Our results suggest that brain size likely explains some of the variation in behavioural plasticity found at the intraspecific level.
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http://dx.doi.org/10.1111/jeb.13405DOI Listing
March 2019

Early neurogenomic response associated with variation in guppy female mate preference.

Nat Ecol Evol 2018 11 8;2(11):1772-1781. Epub 2018 Oct 8.

Department of Genetics, Evolution and Environment, University College London, London, UK.

Understanding the evolution of mate choice requires dissecting the mechanisms of female preference, particularly how these differ among social contexts and preference phenotypes. Here, we studied the female neurogenomic response after only 10 min of mate exposure in both a sensory component (optic tectum) and a decision-making component (telencephalon) of the brain. By comparing the transcriptional response between females with and without preferences for colourful males, we identified unique neurogenomic elements associated with the female preference phenotype that are not present in females without preference. A network analysis revealed different properties for this response at the sensory-processing and the decision-making levels, and we show that this response is highly centralized in the telencephalon. Furthermore, we identified an additional set of genes that vary in expression across social contexts, beyond mate evaluation. We show that transcription factors among these loci are predicted to regulate the transcriptional response of the genes we found to be associated with female preference.
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http://dx.doi.org/10.1038/s41559-018-0682-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6349141PMC
November 2018

Breakdown of brain-body allometry and the encephalization of birds and mammals.

Nat Ecol Evol 2018 09 13;2(9):1492-1500. Epub 2018 Aug 13.

Department of Zoology/Ethology, Stockholm University, Stockholm, Sweden.

The allometric relationship between brain and body size among vertebrates is often considered a manifestation of evolutionary constraints. However, birds and mammals have undergone remarkable encephalization, in which brain size has increased without corresponding changes in body size. Here, we explore the hypothesis that a reduction of phenotypic integration between brain and body size has facilitated encephalization in birds and mammals. Using a large dataset comprising 20,213 specimens across 4,587 species of jawed vertebrates, we show that the among-species (evolutionary) brain-body allometries are remarkably constant, both across vertebrate classes and across taxonomic levels. Birds and mammals, however, are exceptional in that their within-species (static) allometries are shallower and more variable than in other vertebrates. These patterns are consistent with the idea that birds and mammals have reduced allometric constraints that are otherwise ubiquitous across jawed vertebrates. Further exploration of ontogenetic allometries in selected taxa of birds, fishes and mammals reveals that birds and mammals have extended the period of fetal brain growth compared to fishes. Based on these findings, we propose that avian and mammalian encephalization has been contingent on increased variability in brain growth patterns.
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http://dx.doi.org/10.1038/s41559-018-0632-1DOI Listing
September 2018

Selection for relative brain size affects context-dependent male preference for, but not discrimination of, female body size in guppies.

J Exp Biol 2018 06 25;221(Pt 12). Epub 2018 Jun 25.

Department of Zoology/Ethology, Stockholm University, Svante Arrhenius väg 18B, SE-10691 Stockholm, Sweden.

Understanding what drives animal decisions is fundamental in evolutionary biology, and mate choice decisions are arguably some of the most important in any individual's life. As cognitive ability can impact decision making, elucidating the link between mate choice and cognitive ability is necessary to fully understand mate choice. To experimentally study this link, we used guppies () artificially selected for divergence in relative brain size and with previously demonstrated differences in cognitive ability. A previous test in our female guppy selection lines demonstrated the impact of brain size and cognitive ability on information processing during female mate choice decisions. Here, we evaluated the effect of brain size and cognitive ability on male mate choice decisions. Specifically, we investigated the preference of large-brained, small-brained and non-selected guppy males for female body size, a key indicator of female fecundity in this species. For this, male preference was quantified in dichotomous choice tests when presented with dyads of females with small, medium and large body size differences. All types of males showed a preference for larger females but no effect of brain size was found in the ability to discriminate between differently sized females. However, we found that non-selected and large-brained males, but not small-brained males, showed a context-dependent preference for larger females depending on the difference in female size. Our results have two important implications. First, they provide further evidence that male mate choice also occurs in a species in which secondary sexual ornamentation is present only in males. Second, they show that brain size and cognitive ability have important effects on individual variation in mating preference and sexually selected traits.
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http://dx.doi.org/10.1242/jeb.175240DOI Listing
June 2018

Large-brained frogs mature later and live longer.

Evolution 2018 05 24;72(5):1174-1183. Epub 2018 Apr 24.

Zoological Institute, Stockholm University, Stockholm 10691, Sweden.

Brain sizes vary substantially across vertebrate taxa, yet, the evolution of brain size appears tightly linked to the evolution of life histories. For example, larger brained species generally live longer than smaller brained species. A larger brain requires more time to grow and develop at a cost of exceeded gestation period and delayed weaning age. The cost of slower development may be compensated by better homeostasis control and increased cognitive abilities, both of which should increase survival probabilities and hence life span. To date, this relationship between life span and brain size seems well established in homoeothermic animals, especially in mammals. Whether this pattern occurs also in other clades of vertebrates remains enigmatic. Here, we undertake the first comparative test of the relationship between life span and brain size in an ectothermic vertebrate group, the anuran amphibians. After controlling for the effects of shared ancestry and body size, we find a positive correlation between brain size, age at sexual maturation, and life span across 40 species of frogs. Moreover, we also find that the ventral brain regions, including the olfactory bulbs, are larger in long-lived species. Our results indicate that the relationship between life history and brain evolution follows a general pattern across vertebrate clades.
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http://dx.doi.org/10.1111/evo.13478DOI Listing
May 2018

Using activity and sociability to characterize collective motion.

Philos Trans R Soc Lond B Biol Sci 2018 05;373(1746)

Zoology Department, Stockholm University, Stockholm, Sweden.

A wide range of measurements can be made on the collective motion of groups, and the movement of individuals within them. These include, but are not limited to: group size, polarization, speed, turning speed, speed or directional correlations, and distances to near neighbours. From an ecological and evolutionary perspective, we would like to know which of these measurements capture biologically meaningful aspects of an animal's behaviour and contribute to its survival chances. Previous simulation studies have emphasized two main factors shaping individuals' behaviour in groups; attraction and alignment. Alignment responses appear to be important in transferring information between group members and providing synergistic benefits to group members. Likewise, attraction to conspecifics is thought to provide benefits through, for example, selfish herding. Here, we use a factor analysis on a wide range of simple measurements to identify two main axes of collective motion in guppies (): (i) sociability, which corresponds to attraction (and to a lesser degree alignment) to neighbours, and (ii) activity, which combines alignment with directed movement. We show that for guppies, predation in a natural environment produces higher degrees of sociability and (in females) lower degrees of activity, while female guppies sorted for higher degrees of collective alignment have higher degrees of both sociability and activity. We suggest that the activity and sociability axes provide a useful framework for measuring the behaviour of animals in groups, allowing the comparison of individual and collective behaviours within and between species.This article is part of the theme issue 'Collective movement ecology'.
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http://dx.doi.org/10.1098/rstb.2017.0015DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5882985PMC
May 2018

Brain size affects performance in a reversal-learning test.

Proc Biol Sci 2018 01;285(1871)

Department of Zoology/Ethology, Stockholm University, Svante Arrhenius väg 18B, 10691, Stockholm, Sweden.

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 () 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.
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http://dx.doi.org/10.1098/rspb.2017.2031DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5805926PMC
January 2018

Brain size does not impact shoaling dynamics in unfamiliar groups of guppies (Poecilia reticulata).

Behav Processes 2018 Feb 14;147:13-20. Epub 2017 Dec 14.

Department of Zoology, Stockholm University, SE-10691, Stockholm, Sweden.

Collective movement is achieved when individuals adopt local rules to interact with their neighbours. How the brain processes information about neighbours' positions and movements may affect how individuals interact in groups. As brain size can determine such information processing it should impact collective animal movement. Here we investigate whether brain size affects the structure and organisation of newly forming fish shoals by quantifying the collective movement of guppies (Poecilia reticulata) from large- and small-brained selection lines, with known differences in learning and memory. We used automated tracking software to determine shoaling behaviour of single-sex groups of eight or two fish and found no evidence that brain size affected the speed, group size, or spatial and directional organisation of fish shoals. Our results suggest that brain size does not play an important role in how fish interact with each other in these types of moving groups of unfamiliar individuals. Based on these results, we propose that shoal dynamics are likely to be governed by relatively basic cognitive processes that do not differ in these brain size selected lines of guppies.
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http://dx.doi.org/10.1016/j.beproc.2017.12.006DOI Listing
February 2018

On the role of body size, brain size, and eye size in visual acuity.

Behav Ecol Sociobiol 2017;71(12):179. Epub 2017 Nov 29.

Department of Zoology/Ethology, Stockholm University, Svante Arrhenius väg 18B, SE-10691 Stockholm, Sweden.

Abstract: The visual system is highly variable across species, and such variability is a key factor influencing animal behavior. Variation in the visual system, for instance, can influence the outcome of learning tasks when visual stimuli are used. We illustrate this issue in guppies () artificially selected for large and small relative brain size with pronounced behavioral differences in learning experiments and mate choice tests. We performed a study of the visual system by quantifying eye size and optomotor response of large-brained and small-brained guppies. This represents the first experimental test of the link between brain size evolution and visual acuity. We found that female guppies have larger eyes than male guppies, both in absolute terms and in relation to their body size. Likewise, individuals selected for larger brains had slightly larger eyes but not better visual acuity than small-brained guppies. However, body size was positively associated with visual acuity. We discuss our findings in relation to previous macroevolutionary studies on the evolution of brain morphology, eye morphology, visual acuity, and ecological variables, while stressing the importance of accounting for sensory abilities in behavioral studies.

Significance Statement: Pre-existing perceptual biases can be keys for the development of specific behavioral patterns. Hence, potential differences in sensory systems need to be taken into account in the study of animal behavior. We highlight this necessity concentrating on the visual domain and using experimental data on brain size-selected guppies in which we assessed eye size and visual acuity. Behavioral differences between large-brained and small-brained guppies in learning and mate choice predominantly relied on tests using visual cues. Analyses of visual capabilities in this system are therefore necessary. Furthermore, this system offers the unprecedented opportunity to experimentally test the relationship between brain size, eye morphology, and visual capabilities. Our results show similar visual acuities between large-brained and small-brained guppies. However, the differences observed in eye area between the sexes, together with the observed positive relationship between body size and visual acuity, highlight the need to incorporate perceptive differences in the study of animal behavior.
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http://dx.doi.org/10.1007/s00265-017-2408-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5705735PMC
November 2017

Seasonality and brain size are negatively associated in frogs: evidence for the expensive brain framework.

Sci Rep 2017 11 30;7(1):16629. Epub 2017 Nov 30.

Zoological Institute, Stockholm University, 10691, Stockholm, Sweden.

The challenges of seasonal environments are thought to contribute to brain evolution, but in which way is debated. According to the Cognitive Buffer Hypothesis (CBH) brain size should increase with seasonality, as the cognitive benefits of a larger brain should help overcoming periods of food scarcity via, for instance, increased behavioral flexibility. However, in line with the Expensive Brain Framework (EBF) brain size should decrease with seasonality because a smaller brain confers energetic benefits in periods of food scarcity. Empirical evidence is inconclusive and mostly limited to homoeothermic animals. Here we used phylogenetic comparative analyses to test the impact of seasonality on brain evolution across 30 species of anurans (frogs) experiencing a wide range of temperature and precipitation. Our results support the EBF because relative brain size and the size of the optic tectum were negatively correlated with variability in temperature. In contrast, we found no association between the variability in precipitation and the length of the dry season with either brain size or the sizes of other major brain regions. We suggest that seasonality-induced food scarcity resulting from higher variability in temperature constrains brain size evolution in anurans. Less seasonal environments may therefore facilitate the evolution of larger brains in poikilothermic animals.
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http://dx.doi.org/10.1038/s41598-017-16921-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5709389PMC
November 2017

Evolution of brain region volumes during artificial selection for relative brain size.

Evolution 2017 Dec 13;71(12):2942-2951. Epub 2017 Nov 13.

Department of Zoology, Stockholm University, Stockholm, Sweden.

The vertebrate brain shows an extremely conserved layout across taxa. Still, the relative sizes of separate brain regions vary markedly between species. One interesting pattern is that larger brains seem associated with increased relative sizes only of certain brain regions, for instance telencephalon and cerebellum. Till now, the evolutionary association between separate brain regions and overall brain size is based on comparative evidence and remains experimentally untested. Here, we test the evolutionary response of brain regions to directional selection on brain size in guppies (Poecilia reticulata) selected for large and small relative brain size. In these animals, artificial selection led to a fast response in relative brain size, while body size remained unchanged. We use microcomputer tomography to investigate how the volumes of 11 main brain regions respond to selection for larger versus smaller brains. We found no differences in relative brain region volumes between large- and small-brained animals and only minor sex-specific variation. Also, selection did not change allometric scaling between brain and brain region sizes. Our results suggest that brain regions respond similarly to strong directional selection on relative brain size, which indicates that brain anatomy variation in contemporary species most likely stem from direct selection on key regions.
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http://dx.doi.org/10.1111/evo.13373DOI Listing
December 2017

How predation shapes the social interaction rules of shoaling fish.

Proc Biol Sci 2017 Aug;284(1861)

Department of Mathematics, Uppsala University, Uppsala, Sweden.

Predation is thought to shape the macroscopic properties of animal groups, making moving groups more cohesive and coordinated. Precisely how predation has shaped individuals' fine-scale social interactions in natural populations, however, is unknown. Using high-resolution tracking data of shoaling fish () from populations differing in natural predation pressure, we show how predation adapts individuals' social interaction rules. Fish originating from high predation environments formed larger, more cohesive, but not more polarized groups than fish from low predation environments. Using a new approach to detect the discrete points in time when individuals decide to update their movements based on the available social cues, we determine how these collective properties emerge from individuals' microscopic social interactions. We first confirm predictions that predation shapes the attraction-repulsion dynamic of these fish, reducing the critical distance at which neighbours move apart, or come back together. While we find strong evidence that fish align with their near neighbours, we do not find that predation shapes the strength or likelihood of these alignment tendencies. We also find that predation sharpens individuals' acceleration and deceleration responses, implying key perceptual and energetic differences associated with how individuals move in different predation regimes. Our results reveal how predation can shape the social interactions of individuals in groups, ultimately driving differences in groups' collective behaviour.
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http://dx.doi.org/10.1098/rspb.2017.1126DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5577484PMC
August 2017

Sexual selection impacts brain anatomy in frogs and toads.

Ecol Evol 2016 10 12;6(19):7070-7079. Epub 2016 Sep 12.

Zoological Institute Stockholm University Stockholm Sweden.

Natural selection is a major force in the evolution of vertebrate brain size, but the role of sexual selection in brain size evolution remains enigmatic. At least two opposing schools of thought predict a relationship between sexual selection and brain size. Sexual selection should facilitate the evolution of larger brains because better cognitive abilities may aid the competition for mates. However, it may also restrict brain size evolution due to energetic trade-offs between brain tissue and sexually selected traits. Here, we examined the patterns of selection on brain size and brain anatomy in male anurans (frogs and toads), a group where the strength of sexual selection differs markedly among species, using a phylogenetically controlled generalized least-squared (PGLS) regression analyses. The analysis revealed that in 43 Chinese anuran species, neither mating system, nor type of courtship, or testes mass was significantly associated with relative brain size. While none of those factors related to the relative size of olfactory nerves, optic tecta, telencephalon, and cerebellum, the olfactory bulbs were relatively larger in monogamous species and those using calls during courtship. Our findings support the mosaic model of brain evolution and suggest that while the investigated aspects of sexual selection do not seem to play a prominent role in the evolution of brain size of anurans, they do impact their brain anatomy.
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http://dx.doi.org/10.1002/ece3.2459DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5513231PMC
October 2016

Female brain size affects the assessment of male attractiveness during mate choice.

Sci Adv 2017 Mar 22;3(3):e1601990. Epub 2017 Mar 22.

Department of Zoology/Ethology, Stockholm University, Svante Arrhenius väg 18B, SE-10691 Stockholm, Sweden.

Mate choice decisions are central in sexual selection theory aimed to understand how sexual traits evolve and their role in evolutionary diversification. We test the hypothesis that brain size and cognitive ability are important for accurate assessment of partner quality and that variation in brain size and cognitive ability underlies variation in mate choice. We compared sexual preference in guppy female lines selected for divergence in relative brain size, which we have previously shown to have substantial differences in cognitive ability. In a dichotomous choice test, large-brained and wild-type females showed strong preference for males with color traits that predict attractiveness in this species. In contrast, small-brained females showed no preference for males with these traits. In-depth analysis of optomotor response to color cues and gene expression of key opsins in the eye revealed that the observed differences were not due to differences in visual perception of color, indicating that differences in the ability to process indicators of attractiveness are responsible. We thus provide the first experimental support that individual variation in brain size affects mate choice decisions and conclude that differences in cognitive ability may be an important underlying mechanism behind variation in female mate choice.
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http://dx.doi.org/10.1126/sciadv.1601990DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5362185PMC
March 2017

Predation pressure shapes brain anatomy in the wild.

Evol Ecol 2017 12;31(5):619-633. Epub 2017 May 12.

1Department of Ethology/Zoology, Stockholm University, Svante Arheniusväg 18B, 10691 Stockholm, Sweden.

There is remarkable diversity in brain anatomy among vertebrates and evidence is accumulating that predatory interactions are crucially important for this diversity. To test this hypothesis, we collected female guppies () from 16 wild populations and related their brain anatomy to several aspects of predation pressure in this ecosystem, such as the biomass of the four major predators of guppies (one prawn and three fish species), and predator diversity (number of predatory fish species in each site). We found that populations from localities with higher prawn biomass had relatively larger telencephalon size as well as larger brains. Optic tectum size was positively associated with one of the fish predator's biomass and with overall predator diversity. However, both olfactory bulb and hypothalamus size were negatively associated with the biomass of another of the fish predators. Hence, while fish predator occurrence is associated with variation in brain anatomy, prawn occurrence is associated with variation in brain size. Our results suggest that cognitive challenges posed by local differences in predator communities may lead to changes in prey brain anatomy in the wild.
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http://dx.doi.org/10.1007/s10682-017-9901-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6961500PMC
May 2017

Artificial selection on male genitalia length alters female brain size.

Proc Biol Sci 2016 Nov;283(1843)

Department of Zoology/Ethology, Stockholm University, Svante Arrhenius väg 18B, 10691 Stockholm, Sweden.

Male harassment is a classic example of how sexual conflict over mating leads to sex-specific behavioural adaptations. Females often suffer significant costs from males attempting forced copulations, and the sexes can be in an arms race over male coercion. Yet, despite recent recognition that divergent sex-specific interests in reproduction can affect brain evolution, sexual conflict has not been addressed in this context. Here, we investigate whether artificial selection on a correlate of male success at coercion, genital length, affects brain anatomy in males and females. We analysed the brains of eastern mosquitofish (Gambusia holbrooki), which had been artificially selected for long or short gonopodium, thereby mimicking selection arising from differing levels of male harassment. By analogy to how prey species often have relatively larger brains than their predators, we found that female, but not male, brain size was greater following selection for a longer gonopodium. Brain subregion volumes remained unchanged. These results suggest that there is a positive genetic correlation between male gonopodium length and female brain size, which is possibly linked to increased female cognitive ability to avoid male coercion. We propose that sexual conflict is an important factor in the evolution of brain anatomy and cognitive ability.
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http://dx.doi.org/10.1098/rspb.2016.1796DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5136585PMC
November 2016