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  • 1. Bloch, Natasha
    et al.
    Corral-López, Alberto
    Stockholm University, Faculty of Science, Department of Zoology.
    Buechel, Severine D.
    Stockholm University, Faculty of Science, Department of Zoology.
    Kotrschal, Alexander
    Stockholm University, Faculty of Science, Department of Zoology.
    Kolm, Niclas
    Stockholm University, Faculty of Science, Department of Zoology.
    Mank, Judith E.
    Early neurogenomic response associated with variation in guppy female mate preference2018In: Nature Ecology & Evolution, E-ISSN 2397-334X, Vol. 2, no 11, p. 1772-1781Article in journal (Refereed)
    Abstract [en]

    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.

  • 2.
    Corral López, Alberto
    Stockholm University, Faculty of Science, Department of Zoology.
    The link between brain size, cognitive ability, mate choice and sexual behaviour in the guppy (Poecilia reticulata)2017Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    Competition over access for mates has led to the evolution of many striking examples of morphological traits and behaviour in animals. The rapid development of the sexual selection field in recent decades have dramatically advanced our understanding of what traits make individuals more successful in attracting mates and how preferences for mates evolve over time. However, till now, research in this field has put less emphasis on the mechanisms that underlie variation in mate choice and sexual behaviour. Cognitive processes could potentially be key drivers of individual variation in mating preferences and sexual behaviours and therefore deserve further investigation. In this thesis, I used guppies artificially selected for relative brain size as the model system to study the association between brain size, cognitive ability and various aspects of mate choice. Previous studies in this model system showed that large-brained individuals of both sexes outperformed small-brained individuals in cognitive tests. Here I quantified their sexual behaviours and mating preferences to provide novel empirical data concerning the association between brain size, cognitive ability and sexual selection. In dichotomous choice preference tests based on visual cues, comparisons between large-brained and small-brained guppies showed important differences in their assessment of mate quality. These results are not driven by pre-existing visual biases caused by the artificial selection since further investigation of the visual capacity of these fish detected no differences between large-brained and small-brained individuals in their sensitivity to colour or in their capacity to resolve spatial detail. I also quantified sexual behaviour in male guppies artificially selected for relative brain size and found no difference in the behaviours of large-brained and small-brained males in a single male-single female non-competitive scenario. On the contrary, in a more complex social setting I found a reduction in large-brained males in the rate of courtship towards females and dominance displays towards other males when exposed to different degrees of predation threat and different numbers of male competitors. However, this reduction in behavioural intensity did not result in a lower access to copulation with females for large-brained males. I likewise evaluated female sexual behaviour and found that large-brained females had higher behavioural flexibility such that they decreased their receptiveness towards males more strongly under higher levels of predation threat. Together, these results provide novel empirical evidence that brain size and cognitive ability are tightly linked to mating preferences and sexual behaviours. These findings suggest that brain size and cognitive ability might be important mechanisms behind variation in mating preferences and in sexually selected traits across and within species.

  • 3.
    Corral-López, Alberto
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Bloch, Natasha I.
    Kotrschal, Alexander
    Stockholm University, Faculty of Science, Department of Zoology.
    van der Bijl, Wouter
    Stockholm University, Faculty of Science, Department of Zoology.
    Buechel, Severine D.
    Stockholm University, Faculty of Science, Department of Zoology.
    Mank, Judith E.
    Kolm, Niclas
    Stockholm University, Faculty of Science, Department of Zoology.
    Female brain size affects the assessment of male attractiveness during mate choice2017In: Science Advances, ISSN 0036-8156, E-ISSN 2375-2548, Vol. 3, no 3, article id e1601990Article in journal (Refereed)
    Abstract [en]

    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.

  • 4.
    Corral-López, Alberto
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Eckerström-Liedholm, Simon
    Stockholm University, Faculty of Science, Department of Zoology.
    Van der Bijl, Wouter
    Stockholm University, Faculty of Science, Department of Zoology.
    Kotrschal, Alexander
    Stockholm University, Faculty of Science, Department of Zoology.
    Kolm, Niclas
    Stockholm University, Faculty of Science, Department of Zoology.
    No association between brain size and male sexual behavior in the guppy2015In: Current Zoology, ISSN 1674-5507, Vol. 61, no 2, p. 265-273Article in journal (Refereed)
    Abstract [en]

    Animal behavior is remarkably variable at all taxonomic levels. Over the last decades, research on animal behavior has focused on understanding ultimate processes. Yet, it has progressively become more evident that to fully understand behavioral variation, ultimate explanations need to be complemented with proximate ones. In particular, the mechanisms generating variation in sexual behavior remain an open question. Variation in aspects of brain morphology has been suggested as a plausible mechanism underlying this variation. However, our knowledge of this potential association is based almost exclusively on comparative analyses. Experimental studies are needed to establish causality and bridge the gap between micro-and macroevolutionary mechanisms concerning the link between brain and sexual behavior. We used male guppies that had been artificially selected for large or small relative brain size to study this association. We paired males with females and scored the full known set of male and female sexual behaviors described in guppies. We found several previously demonstrated associations between male traits, male behavior and female behavior. Females responded more strongly towards males that courted more and males with more orange coloration. Also, larger males and males with less conspicuous coloration attempted more coerced copulations. However, courting, frequency of coerced copulation attempts, total intensity of sexual behavior, and female response did not differ between large-and small-brained males. Our data suggest that relative brain size is an unlikely mechanism underlying variation in sexual behavior of the male guppy. We discuss these findings in the context of the conditions under which relative brain size might affect male sexual behavior

  • 5.
    Corral-López, Alberto
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Garate-Olaizola, Maddi
    Stockholm University, Faculty of Science, Department of Zoology.
    Buechel, Severine D.
    Stockholm University, Faculty of Science, Department of Zoology.
    Kolm, Niclas
    Stockholm University, Faculty of Science, Department of Zoology.
    Kotrschal, Alexander
    Stockholm University, Faculty of Science, Department of Zoology.
    On the role of body size, brain size, and eye size in visual acuity2017In: Behavioral Ecology and Sociobiology, ISSN 0340-5443, E-ISSN 1432-0762, Vol. 71, no 12, article id UNSP 179Article in journal (Refereed)
    Abstract [en]

    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 (Poecilia reticulata) 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.

  • 6.
    Corral-López, Alberto
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Garate-Olaizola, Maddi
    Buechel, Severine
    Stockholm University, Faculty of Science, Department of Zoology.
    Kolm, Niclas
    Stockholm University, Faculty of Science, Department of Zoology.
    Kotrschal, Alexander
    Stockholm University, Faculty of Science, Department of Zoology.
    On the role of body size, brain size and eye size in visual acuityManuscript (preprint) (Other academic)
  • 7.
    Corral-López, Alberto
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Kotrschal, Alexander
    Stockholm University, Faculty of Science, Department of Zoology.
    Kolm, Niclas
    Stockholm University, Faculty of Science, Department of Zoology.
    Brain size affects the judgment of female quality during male mate choiceManuscript (preprint) (Other academic)
  • 8.
    Corral-López, Alberto
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Kotrschal, Alexander
    Stockholm University, Faculty of Science, Department of Zoology.
    Kolm, Niclas
    Stockholm University, Faculty of Science, Department of Zoology.
    Selection for relative brain size affects context-dependent male preference for, but not discrimination of, female body size in guppies2018In: Journal of Experimental Biology, ISSN 0022-0949, E-ISSN 1477-9145, Vol. 221, no 12, article id jeb175240Article in journal (Refereed)
    Abstract [en]

    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 (Poecilia reticulata) 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 omamentation 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.

  • 9.
    Corral-López, Alberto
    et al.
    Stockholm University, Faculty of Science, Department of Zoology. University College of London, UK.
    Romensky, Maksym
    Kotrschal, Alexander
    Stockholm University, Faculty of Science, Department of Zoology. Wageningen University, The Netherlands.
    Buechel, Severine D.
    Stockholm University, Faculty of Science, Department of Zoology.
    Kolm, Niclas
    Stockholm University, Faculty of Science, Department of Zoology.
    Brain size affects responsiveness in mating behaviour to variation in predation pressure and sex ratio2019In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101Article in journal (Refereed)
    Abstract [en]

    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.

  • 10.
    Corral-López, Alberto
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Romensky, Maksym
    Kotrschal, Alexander
    Stockholm University, Faculty of Science, Department of Zoology.
    Buechel, Severine
    Stockholm University, Faculty of Science, Department of Zoology.
    Kolm, Niclas
    Stockholm University, Faculty of Science, Department of Zoology.
    Brain size, environmental complexity and mating behaviourManuscript (preprint) (Other academic)
  • 11.
    Kotrschal, Alexander
    et al.
    Stockholm University, Faculty of Science, Department of Zoology, Ethology. University of Veterinary Medicine, Austria.
    Buechel, Séverine D.
    Stockholm University, Faculty of Science, Department of Zoology, Ethology. University of Veterinary Medicine, Austria.
    Zala, Sarah M.
    Corral Lopez, Alberto
    Stockholm University, Faculty of Science, Department of Zoology, Ethology.
    Penn, Dustin J.
    Kolm, Niclas
    Stockholm University, Faculty of Science, Department of Zoology, Ethology.
    Brain size affects female but not male survival under predation threat2015In: Ecology Letters, ISSN 1461-023X, E-ISSN 1461-0248, Vol. 18, no 7, p. 646-652Article in journal (Refereed)
    Abstract [en]

    There is remarkable diversity in brain size among vertebrates, but surprisingly little is known about how ecological species interactions impact the evolution of brain size. Using guppies, artificially selected for large and small brains, we determined how brain size affects survival under predation threat in a naturalistic environment. We cohoused mixed groups of small- and large-brained individuals in six semi-natural streams with their natural predator, the pike cichlid, and monitored survival in weekly censuses over 5 months. We found that large-brained females had 13.5% higher survival compared to small-brained females, whereas the brain size had no discernible effect on male survival. We suggest that large-brained females have a cognitive advantage that allows them to better evade predation, whereas large-brained males are more colourful, which may counteract any potential benefits of brain size. Our study provides the first experimental evidence that trophic interactions can affect the evolution of brain size.

  • 12.
    Kotrschal, Alexander
    et al.
    Stockholm University, Faculty of Science, Department of Zoology, Ethology. Uppsala University, Sweden.
    Corral-Lopez, Alberto
    Stockholm University, Faculty of Science, Department of Zoology, Ethology.
    Amcoff, Mirjam
    Kolm, Niclas
    Stockholm University, Faculty of Science, Department of Zoology, Ethology. Uppsala University, Sweden.
    A larger brain confers a benefit in a spatial mate search learning task in male guppies2015In: Behavioral Ecology, ISSN 1045-2249, E-ISSN 1465-7279, Vol. 26, no 2, p. 527-532Article in journal (Refereed)
    Abstract [en]

    Brain size varies dramatically among vertebrates, and selection for increased cognitive abilities is thought to be the key force underlying the evolution of a large brain. Indeed, numerous comparative studies suggest positive relationships between cognitively demanding aspects of behavior and brain size controlled for body size. However, experimental evidence for the link between relative brain size and cognitive ability is surprisingly scarce and to date stems from a single study on brain size selected guppies (Poecilia reticulata), where large-brained females were shown to outperform small-brained females in a numerical learning assay. Because the results were inconclusive for males in that study, we here use a more ecologically relevant test of male cognitive ability to investigate whether or not a relatively larger brain increases cognitive ability also in males. We compared mate search ability of these artificially selected large-and small-brained males in a maze and found that large-brained males were faster at learning to find a female in a maze. Large-brained males decreased the time spent navigating the maze faster than small-brained males and were nearly twice as fast through the maze after 2 weeks of training. Our results support that relatively larger brains are better also for males in some contexts, which further substantiates that variation in vertebrate brain size is generated through the balance between energetic costs and cognitive benefits.

  • 13.
    Kotrschal, Alexander
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Corral-Lopez, Alberto
    Stockholm University, Faculty of Science, Department of Zoology.
    Kolm, Niclas
    Stockholm University, Faculty of Science, Department of Zoology.
    Large brains, short life: selection on brain size impacts intrinsic lifespan2019In: Biology Letters, ISSN 1744-9561, E-ISSN 1744-957X, Vol. 15, no 5, article id 20190137Article in journal (Refereed)
    Abstract [en]

    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.

  • 14.
    Kotrschal, Alexander
    et al.
    Stockholm University, Faculty of Science, Department of Zoology, Ethology.
    Corral-Lopez, Alberto
    Stockholm University, Faculty of Science, Department of Zoology, Ethology.
    Szidat, Soenke
    Kolm, Niclas
    Stockholm University, Faculty of Science, Department of Zoology, Ethology.
    The effect of brain size evolution on feeding propensity, digestive efficiency, and juvenile growth2015In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 69, no 11, p. 3013-3020Article in journal (Refereed)
    Abstract [en]

    One key hypothesis in the study of brain size evolution is the expensive tissue hypothesis; the idea that increased investment into the brain should be compensated by decreased investment into other costly organs, for instance the gut. Although the hypothesis is supported by both comparative and experimental evidence, little is known about the potential changes in energetic requirements or digestive traits following such evolutionary shifts in brain and gut size. Organisms may meet the greater metabolic requirements of larger brains despite smaller guts via increased food intake or better digestion. But increased investment in the brain may also hamper somatic growth. To test these hypotheses we here used guppy (Poecilia reticulata) brain size selection lines with a pronounced negative association between brain and gut size and investigated feeding propensity, digestive efficiency (DE), and juvenile growth rate. We did not find any difference in feeding propensity or DE between large-and small-brained individuals. Instead, we found that large-brained females had slower growth during the first 10 weeks after birth. Our study provides experimental support that investment into larger brains at the expense of gut tissue carries costs that are not necessarily compensated by a more efficient digestive system.

  • 15.
    Kotrschal, Alexander
    et al.
    Stockholm University, Faculty of Science, Department of Zoology. Uppsala University, Sweden.
    Corral-Lopez, Alberto
    Stockholm University, Faculty of Science, Department of Zoology.
    Zajitschek, S.
    Immler, S.
    Maklakov, A. A.
    Kolm, Niclas
    Stockholm University, Faculty of Science, Department of Zoology.
    Positive genetic correlation between brain size and sexual traits in male guppies artificially selected for brain size2015In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 28, no 4, p. 841-850Article in journal (Refereed)
    Abstract [en]

    Brain size is an energetically costly trait to develop and maintain. Investments into other costly aspects of an organism's biology may therefore place important constraints on brain size evolution. Sexual traits are often costly and could therefore be traded off against neural investment. However, brain size may itself be under sexual selection through mate choice on cognitive ability. Here, we use guppy (Poecilia reticulata) lines selected for large and small brain size relative to body size to investigate the relationship between brain size, a large suite of male primary and secondary sexual traits, and body condition index. We found no evidence for trade-offs between brain size and sexual traits. Instead, larger-brained males had higher expression of several primary and precopulatory sexual traits - they had longer genitalia, were more colourful and developed longer tails than smaller-brained males. Larger-brained males were also in better body condition when housed in single-sex groups. There was no difference in post-copulatory sexual traits between males from the large- and small-brained lines. Our data do not support the hypothesis that investment into sexual traits is an important limiting factor to brain size evolution, but instead suggest that brain size and several sexual traits are positively genetically correlated.

  • 16. Outomuro, David
    et al.
    Angel-Giraldo, Pedro
    Corral-López, Alberto
    Stockholm University, Faculty of Science, Department of Zoology.
    Realpe, Emilio
    Multitrait aposematic signal in Batesian mimicry2016In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 70, no 7, p. 1596-1608Article in journal (Refereed)
    Abstract [en]

    Batesian mimics can parasitize Mullerian mimicry rings mimicking the warning color signal. The evolutionary success of Batesian mimics can increase adding complexity to the signal by behavioral and locomotor mimicry. We investigated three fundamental morphological and locomotor traits in a Neotropical mimicry ring based on Ithomiini butterflies and parasitized by Polythoridae damselflies: wing color, wing shape, and flight style. The study species have wings with a subapical white patch, considered the aposematic signal, and a more apical black patch. The main predators are VS-birds, visually more sensitive to violet than to ultraviolet wavelengths (UVS-birds). The white patches, compared to the black patches, were closer in the bird color space, with higher overlap for VS-birds than for UVS-birds. Using a discriminability index for bird vision, the white patches were more similar between the mimics and the model than the black patches. The wing shape of the mimics was closer to the model in the morphospace, compared to other outgroup damselflies. The wing-beat frequency was similar among mimics and the model, and different from another outgroup damselfly. Multitrait aposematic signals involving morphology and locomotion may favor the evolution of mimicry rings and the success of Batesian mimics by improving signal effectiveness toward predators.

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