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  • 1. Barribeau, Seth M.
    et al.
    Sadd, Ben M.
    du Plessis, Louis
    Brown, Mark J. F.
    Buechel, Severine D.
    Institute of Integrative Biology, Switzerland.
    Cappelle, Kaat
    Carolan, James C.
    Christiaens, Olivier
    Colgan, Thomas J.
    Erler, Silvio
    Evans, Jay
    Helbing, Sophie
    Karaus, Elke
    Lattorff, H. Michael G.
    Marxer, Monika
    Meeus, Ivan
    Näpflin, Kathrin
    Niu, Jinzhi
    Schmid-Hempel, Regula
    Smagghe, Guy
    Waterhouse, Robert M.
    Yu, Na
    Zdobnov, Evgeny M.
    Schmid-Hempel, Paul
    A depauperate immune repertoire precedes evolution of sociality in bees2015In: Genome Biology, ISSN 1465-6906, E-ISSN 1474-760X, Vol. 16, no 83Article in journal (Refereed)
    Abstract [en]

    BACKGROUND: Sociality has many rewards, but can also be dangerous, as high population density and low genetic diversity, common in social insects, is ideal for parasite transmission. Despite this risk, honeybees and other sequenced social insects have far fewer canonical immune genes relative to solitary insects. Social protection from infection, including behavioral responses, may explain this depauperate immune repertoire. Here, based on full genome sequences, we describe the immune repertoire of two ecologically and commercially important bumblebee species that diverged approximately 18 million years ago, the North American Bombus impatiens and European Bombus terrestris.

    RESULTS: We find that the immune systems of these bumblebees, two species of honeybee, and a solitary leafcutting bee, are strikingly similar. Transcriptional assays confirm the expression of many of these genes in an immunological context and more strongly in young queens than males, affirming Bateman's principle of greater investment in female immunity. We find evidence of positive selection in genes encoding antiviral responses, components of the Toll and JAK/STAT pathways, and serine protease inhibitors in both social and solitary bees. Finally, we detect many genes across pathways that differ in selection between bumblebees and honeybees, or between the social and solitary clades.

    CONCLUSIONS: The similarity in immune complement across a gradient of sociality suggests that a reduced immune repertoire predates the evolution of sociality in bees. The differences in selection on immune genes likely reflect divergent pressures exerted by parasites across social contexts.

  • 2. 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.

  • 3.
    Buechel, Severine Denise
    et al.
    Stockholm University, Faculty of Science, Department of Zoology. ETH Zurich, Switzerland.
    Schmid-Hempel, Paul
    Colony pace: a life-history trait affecting social insect epidemiology2016In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 283, no 1822, article id 20151919Article in journal (Refereed)
    Abstract [en]

    Among colonies of social insects, the worker turnover rate (colony 'pace') typically shows considerable variation. This has epidemiological consequences for parasites, because in 'fast-paced' colonies, with short-lived workers, the time of parasite residence in a given host will be reduced, and further transmission may thus get less likely. Here, we test this idea and ask whether pace is a life-history strategy against infectious parasites. We infected bumblebees (Bombus terrestris) with the infectious gut parasite Crithidia bombi, and experimentally manipulated birth and death rates to mimic slow and fast pace. We found that fewer workers and, importantly, fewer last-generation workers that are responsible for rearing sexuals were infected in colonies with faster pace. This translates into increased fitness in fast-paced colonies, as daughter queens exposed to fewer infected workers in the nest are less likely to become infected themselves, and have a higher chance of founding their own colonies in the next year. High worker turnover rate can thus act as a strategy of defence against a spreading infection in social insect colonies.

  • 4.
    Buechel, Séverine D.
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Booksmythe, Isobel
    Kotrschal, Alexander
    Stockholm University, Faculty of Science, Department of Zoology.
    Jennions, Michael D.
    Kolm, Niclas
    Stockholm University, Faculty of Science, Department of Zoology.
    Artificial selection on male genitalia length alters female brain size2016In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 283, no 1843, article id 20161796Article in journal (Refereed)
    Abstract [en]

    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.

  • 5.
    Buechel, Séverine D.
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Noreikiene, Kristina
    DeFaveri, Jacquelin
    Toli, Elisavet
    Kolm, Niclas
    Stockholm University, Faculty of Science, Department of Zoology.
    Merilä, Juha
    Variation in sexual brain size dimorphism over the breeding cycle in the three-spined stickleback2019In: Journal of Experimental Biology, ISSN 0022-0949, E-ISSN 1477-9145, Vol. 222, no 7, article id UNSP jeb194464Article in journal (Refereed)
    Abstract [en]

    Snapshot analyses have demonstrated dramatic intraspecific variation in the degree of brain sexual size dimorphism (SSD). Although brain SSDis believed to be generated by the sex-specific cognitive demands of reproduction, the relative roles of developmental and population-specific contributions to variation in brain SSD remain little studied. Using a common garden experiment, we tested for sex-specific changes in brain anatomy over the breeding cycle in three-spined stickleback (Gasterosteus aculeatus) sampled from four locations in northern Europe. We found that the male brain increased in size (ca. 24%) significantly more than the female brain towards breeding, and that the resulting brain SSD was similar (ca. 20%) for all populations over the breeding cycle. Our findings support the notion that the stickleback brain is highly plastic and changes over the breeding cycle, especially in males, likely as an adaptive response to the cognitive demands of reproduction (e.g. nest construction and parental care). The results also provide evidence to suggest that breeding-related changes in brain size may be the reason for the widely varying estimates of brain SSD across studies of this species, cautioning against interpreting brain size measurements from a single time point as fixed/static.

  • 6.
    Buechel, Séverine D.
    et al.
    University of Lausanne, Switzerland; Institute of Integrative Biology (IBZ), Switzerland.
    Wurm, Yanick
    Keller, Laurent
    Social chromosome variants differentially affect queen determination and the survival of workers in the fire ant Solenopsis invicta2014In: Molecular Ecology, ISSN 0962-1083, E-ISSN 1365-294X, Vol. 23, no 20, p. 5117-5127Article in journal (Refereed)
    Abstract [en]

    Intraspecific variation in social organization is common, yet the underlying causes are rarely known. An exception is the fire ant Solenopsis invicta in which the existence of two distinct forms of social colony organization is under the control of the two variants of a pair of social chromosomes, SB and Sb. Colonies containing exclusively SB/SB workers accept only one single queen and she must be SB/SB. By contrast, when colonies contain more than 10% of SB/Sb workers, they accept several queens but only SB/Sb queens. The variants of the social chromosome are associated with several additional important phenotypic differences, including the size, fecundity and dispersal strategies of queens, aggressiveness of workers, and sperm count in males. However, little is known about whether social chromosome variants affect fitness in other life stages. Here, we perform experiments to determine whether differential selection occurs during development and in adult workers. We find evidence that the Sb variant of the social chromosome increases the likelihood of female brood to develop into queens and that adult SB/Sb workers, the workers that cull SB/SB queens, are overrepresented in comparison to SB/SB workers. This demonstrates that supergenes such as the social chromosome can have complex effects on phenotypes at various stages of development.

  • 7. Burger, Joep M. S.
    et al.
    Buechel, Séverine D.
    University of Lausanne, Switzerland.
    Kawecki, Tadeusz J.
    Dietary restriction affects lifespan but not cognitive aging in Drosophila melanogaster2010In: Aging Cell, ISSN 1474-9718, E-ISSN 1474-9726, Vol. 9, no 3, p. 327-335Article in journal (Refereed)
    Abstract [en]

    Dietary restriction extends lifespan in a wide variety of animals, including Drosophila, but its relationship to functional and cognitive aging is unclear. Here, we study the effects of dietary yeast content on fly performance in an aversive learning task (association between odor and mechanical shock). Learning performance declined at old age, but 50-day-old dietary-restricted flies learned as poorly as equal-aged flies maintained on yeast-rich diet, even though the former lived on average 9 days (14%) longer. Furthermore, at the middle age of 21 days, flies on low-yeast diets showed poorer short-term (5 min) memory than flies on rich diet. In contrast, dietary restriction enhanced 60-min memory of young (5 days old) flies. Thus, while dietary restriction had complex effects on learning performance in young to middle-aged flies, it did not attenuate aging-related decline of aversive learning performance. These results are consistent with the hypothesis that, in Drosophila, dietary restriction reduces mortality and thus leads to lifespan extension, but does not affect the rate with which somatic damage relevant for cognitive performance accumulates with age.

  • 8. Cauchoix, M.
    et al.
    Chow, P. K. Y.
    van Horik, J. O.
    Atance, C. M.
    Barbeau, E. J.
    Barragan-Jason, G.
    Bize, P.
    Boussard, Annika
    Stockholm University, Faculty of Science, Department of Zoology.
    Buechel, Severine D.
    Stockholm University, Faculty of Science, Department of Zoology.
    Cabirol, A.
    Cauchard, L.
    Claidiere, N.
    Dalesman, S.
    Devaud, J. M.
    Didic, M.
    Doligez, B.
    Fagot, J.
    Fichtel, C.
    Henke-von der Malsburg, J.
    Hermer, E.
    Huber, L.
    Huebner, F.
    Kappeler, P. M.
    Klein, S.
    Langbein, J.
    Langley, E. J. G.
    Lea, S. E. G.
    Lihoreau, M.
    Lovlie, H.
    Matzel, L. D.
    Nakagawa, S.
    Nawroth, C.
    Oesterwind, S.
    Sauce, B.
    Smith, E. A.
    Sorato, E.
    Tebbich, S.
    Wallis, L. J.
    Whiteside, M. A.
    Wilkinson, A.
    Chaine, A. S.
    Morand-Ferron, J.
    The repeatability of cognitive performance: a meta-analysis2018In: Philosophical Transactions of the Royal Society of London. Biological Sciences, ISSN 0962-8436, E-ISSN 1471-2970, Vol. 373, no 1756, article id 20170281Article in journal (Refereed)
    Abstract [en]

    Behavioural and cognitive processes play important roles in mediating an individual's interactions with its environment. Yet, while there is a vast literature on repeatable individual differences in behaviour, relatively little is known about the repeatability of cognitive performance. To further our understanding of the evolution of cognition, we gathered 44 studies on individual performance of 25 species across six animal classes and used meta-analysis to assess whether cognitive performance is repeatable. We compared repeatability (R) in performance (1) on the same task presented at different times (temporal repeatability), and (2) on different tasks that measured the same putative cognitive ability (contextual repeatability). We also addressed whether R estimates were influenced by seven extrinsic factors (moderators): type of cognitive performance measurement, type of cognitive task, delay between tests, origin of the subjects, experimental context, taxonomic class and publication status. We found support for both temporal and contextual repeatability of cognitive performance, with mean R estimates ranging between 0.15 and 0.28. Repeatability estimates were mostly influenced by the type of cognitive performance measures and publication status. Our findings highlight the widespread occurrence of consistent inter-individual variation in cognition across a range of taxa which, like behaviour, may be associated with fitness outcomes. This article is part of the theme issue 'Causes and consequences of individual differences in cognitive abilities'.

  • 9.
    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.

  • 10.
    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.

  • 11.
    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)
  • 12.
    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 ratio2020In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 33, no 2, p. 165-177Article 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.

  • 13.
    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)
  • 14.
    Fong, Stephanie
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Buechel, Séverine D.
    Stockholm University, Faculty of Science, Department of Zoology.
    Boussard, Annika
    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.
    Plastic changes in brain morphology in relation to learning and environmental enrichment in the guppy (Poecilia reticulata)2019In: Journal of Experimental Biology, ISSN 0022-0949, E-ISSN 1477-9145, Vol. 222, no 10, article id UNSP jeb200402Article in journal (Refereed)
    Abstract [en]

    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.

  • 15. Hayward, A.
    et al.
    Tsuboi, M.
    Owusu, C.
    Kotrschal, Alexander
    Stockholm University, Faculty of Science, Department of Zoology.
    Buechel, Severine D.
    Stockholm University, Faculty of Science, Department of Zoology.
    Zidar, J.
    Cornwallis, C. K.
    Lovlie, H.
    Kolm, Niclas
    Stockholm University, Faculty of Science, Department of Zoology.
    Evolutionary associations between host traits and parasite load: insights from Lake Tanganyika cichlids2017In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 30, no 6, p. 1056-1067Article in journal (Refereed)
    Abstract [en]

    Parasite diversity and abundance (parasite load) vary greatly among host species. However, the influence of host traits on variation in parasitism remains poorly understood. Comparative studies of parasite load have largely examined measures of parasite species richness and are predominantly based on records obtained from published data. Consequently, little is known about the relationships between host traits and other aspects of parasite load, such as parasite abundance, prevalence and aggregation. Meanwhile, understanding of parasite species richness may be clouded by limitations associated with data collation from multiple independent sources. We conducted a field study of Lake Tanganyika cichlid fishes and their helminth parasites. Using a Bayesian phylogenetic comparative framework, we tested evolutionary associations between five key host traits (body size, gut length, diet breadth, habitat complexity and number of sympatric hosts) predicted to influence parasitism, together with multiple measures of parasite load. We find that the number of host species that a particular host may encounter due to its habitat preferences emerges as a factor of general importance for parasite diversity, abundance and prevalence, but not parasite aggregation. In contrast, body size and gut size are positively related to aspects of parasite load within, but not between species. The influence of host phylogeny varies considerably among measures of parasite load, with the greatest influence exerted on parasite diversity. These results reveal that both host morphology and biotic interactions are key determinants of host-parasite associations and that consideration of multiple aspects of parasite load is required to fully understand patterns in parasitism.

  • 16.
    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.

  • 17.
    Kotrschal, Alexander
    et al.
    Stockholm University, Faculty of Science, Department of Zoology.
    Szorkovszky, Alexander
    Romenskyy, Maksym
    Perna, Andrea
    Buechel, Severine D.
    Stockholm University, Faculty of Science, Department of Zoology.
    Zeng, Hong-Li
    Pelckmans, Kristiaan
    Sumpter, David
    Kolm, Niclas
    Stockholm University, Faculty of Science, Department of Zoology.
    Brain size does not impact shoaling dynamics in unfamiliar groups of guppies (Poecilia reticulata)2018In: Behavioural Processes, ISSN 0376-6357, E-ISSN 1872-8308, Vol. 147, p. 13-20Article in journal (Refereed)
    Abstract [en]

    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.

  • 18. Reber, A
    et al.
    Purcell, J
    Buechel, S D
    Buri, P
    Chapuisat, M
    The expression and impact of antifungal grooming in ants.2011In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 24, no 5, p. 954-64Article in journal (Refereed)
    Abstract [en]

    Parasites can cause extensive damage to animal societies in which many related individuals frequently interact. In response, social animals have evolved diverse individual and collective defences. Here, we measured the expression and efficiency of self-grooming and allo-grooming when workers of the ant Formica selysi were contaminated with spores of the fungal entomopathogen Metarhizium anisopliae. The amount of self-grooming increased in the presence of fungal spores, which shows that the ants are able to detect the risk of infection. In contrast, the amount of allo-grooming did not depend on fungal contamination. Workers groomed all nestmate workers that were re-introduced into their groups. The amount of allo-grooming towards noncontaminated individuals was higher when the group had been previously exposed to the pathogen. Allo-grooming decreased the number of fungal spores on the surface of contaminated workers, but did not prevent infection in the conditions tested (high dose of spores and late allo-grooming). The rate of disease transmission to groomers and other nestmates was extremely low. The systematic allo-grooming of all individuals returning to the colony, be they contaminated or not, is probably a simple but robust prophylactic defence preventing the spread of fungal diseases in insect societies.

  • 19. Sadd, Ben M.
    et al.
    Barribeau, Seth M.
    Bloch, Guy
    de Graaf, Dirk C.
    Dearden, Peter
    Elsik, Christine G.
    Gadau, Jürgen
    Grimmelikhuijzen, Cornelis J. P.
    Hasselmann, Martin
    Lozier, Jeffrey D.
    Robertson, Hugh M.
    Smagghe, Guy
    Stolle, Eckart
    Van Vaerenbergh, Matthias
    Waterhouse, Robert M.
    Bornberg-Bauer, Erich
    Klasberg, Steffen
    Bennett, Anna K.
    Câmara, Francisco
    Guigó, Roderic
    Hoff, Katharina
    Mariotti, Marco
    Munoz-Torres, Monica
    Murphy, Terence
    Santesmasses, Didac
    Amdam, Gro V.
    Beckers, Matthew
    Beye, Martin
    Biewer, Matthias
    Bitondi, Márcia M. G.
    Blaxter, Mark L.
    Bourke, Andrew F. G.
    Brown, Mark J. F.
    Buechel, Severine D.
    Eidgenössiche Technische Hochschule (ETH), Switzerland.
    Cameron, Rossanah
    Cappelle, Kaat
    Carolan, James C.
    Christiaens, Olivier
    Ciborowski, Kate L.
    Clarke, David F.
    Colgan, Thomas J.
    Collins, David H.
    Cridge, Andrew G.
    Dalmay, Tamas
    Dreier, Stephanie
    du Plessis, Louis
    Duncan, Elizabeth
    Erler, Silvio
    Evans, Jay
    Falcon, Tiago
    Flores, Kevin
    Freitas, Flávia C. P.
    Fuchikawa, Taro
    Gempe, Tanja
    Hartfelder, Klaus
    Hauser, Frank
    Helbing, Sophie
    Humann, Fernanda C.
    Irvine, Frano
    Jermiin, Lars S.
    Johnson, Claire E.
    Johnson, Reed M.
    Jones, Andrew K.
    Kadowaki, Tatsuhiko
    Kidner, Jonathan H.
    Koch, Vasco
    Köhler, Arian
    Kraus, F. Bernhard
    Lattorff, H. Michael G.
    Leask, Megan
    Lockett, Gabrielle A.
    Mallon, Eamonn B.
    Antonio, David S. Marco
    Marxer, Monika
    Meeus, Ivan
    Moritz, Robin F. A.
    Nair, Ajay
    Näpflin, Kathrin
    Nissen, Inga
    Niu, Jinzhi
    Nunes, Francis M. F.
    Oakeshott, John G.
    Osborne, Amy
    Otte, Marianne
    Pinheiro, Daniel G.
    Rossié, Nina
    Rueppell, Olav
    Santos, Carolina G.
    Schmid-Hempel, Regula
    Schmitt, Björn D.
    Schulte, Christina
    Simões, Zilá L. P.
    Soares, Michelle P. M.
    Swevers, Luc
    Winnebeck, Eva C.
    Wolschin, Florian
    Yu, Na
    Zdobnov, Evgeny M.
    Aqrawi, Peshtewani K.
    Blankenburg, Kerstin P.
    Coyle, Marcus
    Francisco, Liezl
    Hernandez, Alvaro G.
    Holder, Michael
    Hudson, Matthew E.
    Jackson, LaRonda
    Jayaseelan, Joy
    Joshi, Vandita
    Kovar, Christie
    Lee, Sandra L.
    Mata, Robert
    Mathew, Tittu
    Newsham, Irene F.
    Ngo, Robin
    Okwuonu, Geoffrey
    Pham, Christopher
    Pu, Ling-Ling
    Saada, Nehad
    Santibanez, Jireh
    Simmons, DeNard
    Thornton, Rebecca
    Venkat, Aarti
    Walden, Kimberly Ko
    Wu, Yuan-Qing
    Debyser, Griet
    Devreese, Bart
    Asher, Claire
    Blommaert, Julie
    Chipman, Ariel D.
    Chittka, Lars
    Fouks, Bertrand
    Liu, Jisheng
    O'Neill, Meaghan P.
    Sumner, Seirian
    Puiu, Daniela
    Qu, Jiaxin
    Salzberg, Steven L.
    Scherer, Steven E.
    Muzny, Donna M.
    Richards, Stephen
    Robinson, Gene E.
    Gibbs, Richard A.
    Schmid-Hempel, Paul
    Worley, Kim C.
    The genomes of two key bumblebee species with primitive eusocial organization2015In: Genome Biology, ISSN 1465-6906, E-ISSN 1474-760X, Vol. 16, no 76Article in journal (Refereed)
    Abstract [en]

    BACKGROUND: The shift from solitary to social behavior is one of the major evolutionary transitions. Primitively eusocial bumblebees are uniquely placed to illuminate the evolution of highly eusocial insect societies. Bumblebees are also invaluable natural and agricultural pollinators, and there is widespread concern over recent population declines in some species. High-quality genomic data will inform key aspects of bumblebee biology, including susceptibility to implicated population viability threats.

    RESULTS: We report the high quality draft genome sequences of Bombus terrestris and Bombus impatiens, two ecologically dominant bumblebees and widely utilized study species. Comparing these new genomes to those of the highly eusocial honeybee Apis mellifera and other Hymenoptera, we identify deeply conserved similarities, as well as novelties key to the biology of these organisms. Some honeybee genome features thought to underpin advanced eusociality are also present in bumblebees, indicating an earlier evolution in the bee lineage. Xenobiotic detoxification and immune genes are similarly depauperate in bumblebees and honeybees, and multiple categories of genes linked to social organization, including development and behavior, show high conservation. Key differences identified include a bias in bumblebee chemoreception towards gustation from olfaction, and striking differences in microRNAs, potentially responsible for gene regulation underlying social and other traits.

    CONCLUSIONS: These two bumblebee genomes provide a foundation for post-genomic research on these key pollinators and insect societies. Overall, gene repertoires suggest that the route to advanced eusociality in bees was mediated by many small changes in many genes and processes, and not by notable expansion or depauperation.

  • 20. Szorkovszky, Alex
    et al.
    Kotrschal, Alexander
    Stockholm University, Faculty of Science, Department of Zoology. Stockholm Univ, Zool Dept, Stockholm, Sweden.
    Herbert-Read, James E.
    Stockholm University, Faculty of Science, Department of Zoology. University of Bristol, U.K..
    Buechel, Severine D.
    Stockholm University, Faculty of Science, Department of Zoology.
    Romenskyy, Maksym
    Rosen, Emil
    van der Bijl, Wouter
    Stockholm University, Faculty of Science, Department of Zoology.
    Pelckmans, Kristiaan
    Kolm, Niclas
    Stockholm University, Faculty of Science, Department of Zoology.
    Sumpter, David J. T.
    Assortative interactions revealed by sorting of animal groups2018In: Animal Behaviour, ISSN 0003-3472, E-ISSN 1095-8282, Vol. 142, p. 165-179Article in journal (Refereed)
    Abstract [en]

    Animals living in groups can show substantial variation in social traits and this affects their social organization. However, as the specific mechanisms driving this organization are difficult to identify in already organized groups typically found in the wild, the contribution of interindividual variation to group level behaviour remains enigmatic. Here, we present results of an experiment to create and compare groups that vary in social organization, and study how individual behaviour varies between these groups. We iteratively sorted individuals between groups of guppies, Poecilia reticulata, by ranking the groups according to their directional alignment and then mixing similar groups. Over the rounds of sorting the consistency of the group rankings increased, producing groups that varied significantly in key social behaviours such as collective activity and group cohesion. The repeatability of the underlying individual behaviour was then estimated by comparing the experimental data to simulations. At the level of basic locomotion, individuals in more coordinated groups displayed stronger interactions with the centre of the group, and weaker interactions with their nearest neighbours. We propose that this provides the basis for a passive phenotypic assortment mechanism that may explain the structures of social networks in the wild.

  • 21. Tsuboi, Masahito
    et al.
    Husby, Arild
    Kotrschal, Alexander
    Stockholm University, Faculty of Science, Department of Zoology, Ethology.
    Hayward, Alexander
    Stockholm University, Faculty of Science, Department of Zoology, Ethology.
    Buechel, Severine D.
    ETH Zürich Institute of Integrative Biology (IBZ), Switzerland.
    Zidar, Josefina
    Lovlie, Hanne
    Kolm, Niclas
    Stockholm University, Faculty of Science, Department of Zoology, Ethology.
    Comparative support for the expensive tissue hypothesis: Big brains are correlated with smaller gut and greater parental investment in Lake Tanganyika cichlids2015In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 69, no 1, p. 190-200Article in journal (Refereed)
    Abstract [en]

    The brain is one of the most energetically expensive organs in the vertebrate body. Consequently, the energetic requirements of encephalization are suggested to impose considerable constraints on brain size evolution. Three main hypotheses concerning how energetic constraints might affect brain evolution predict covariation between brain investment and (1) investment into other costly tissues, (2) overall metabolic rate, and (3) reproductive investment. To date, these hypotheses have mainly been tested in homeothermic animals and the existing data are inconclusive. However, there are good reasons to believe that energetic limitations might play a role in large-scale patterns of brain size evolution also in ectothermic vertebrates. Here, we test these hypotheses in a group of ectothermic vertebrates, the Lake Tanganyika cichlid fishes. After controlling for the effect of shared ancestry and confounding ecological variables, we find a negative association between brain size and gut size. Furthermore, we find that the evolution of a larger brain is accompanied by increased reproductive investment into egg size and parental care. Our results indicate that the energetic costs of encephalization may be an important general factor involved in the evolution of brain size also in ectothermic vertebrates.

  • 22. Tsuboi, Masahito
    et al.
    Kotrschal, Alexander
    Stockholm University, Faculty of Science, Department of Zoology.
    Hayward, Alexander
    Stockholm University, Faculty of Science, Department of Zoology.
    Buechel, Severine Denise
    Stockholm University, Faculty of Science, Department of Zoology.
    Zidar, Josefina
    Lovlie, Hanne
    Kolm, Niclas
    Stockholm University, Faculty of Science, Department of Zoology.
    Evolution of brain-body allometry in Lake Tanganyika cichlids2016In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 70, no 7, p. 1559-1568Article in journal (Refereed)
    Abstract [en]

    Brain size is strongly associated with body size in all vertebrates. This relationship has been hypothesized to be an important constraint on adaptive brain size evolution. The essential assumption behind this idea is that static (i.e., within species) brain-body allometry has low ability to evolve. However, recent studies have reported mixed support for this view. Here, we examine brain-body static allometry in Lake Tanganyika cichlids using a phylogenetic comparative framework. We found considerable variation in the static allometric intercept, which explained the majority of variation in absolute and relative brain size. In contrast, the slope of the brain-body static allometry had relatively low variation, which explained less variation in absolute and relative brain size compared to the intercept and body size. Further examination of the tempo and mode of evolution of static allometric parameters confirmed these observations. Moreover, the estimated evolutionary parameters indicate that the limited observed variation in the static allometric slope could be a result of strong stabilizing selection. Overall, our findings suggest that the brain-body static allometric slope may represent an evolutionary constraint in Lake Tanganyika cichlids.

  • 23. Wright, Alison E.
    et al.
    Darolti, Iulia
    Bloch, Natasha I.
    Oostra, Vicencio
    Sandkam, Ben
    Buechel, Severine D.
    Stockholm University, Faculty of Science, Department of Zoology.
    Kolm, Niclas
    Stockholm University, Faculty of Science, Department of Zoology.
    Breden, Felix
    Vicoso, Beatriz
    Mank, Judith E.
    Convergent recombination suppression suggests role of sexual selection in guppy sex chromosome formation2017In: Nature Communications, ISSN 2041-1723, E-ISSN 2041-1723, Vol. 8, article id 14251Article in journal (Refereed)
    Abstract [en]

    Sex chromosomes evolve once recombination is halted between a homologous pair of chromosomes. The dominant model of sex chromosome evolution posits that recombination is suppressed between emerging X and Y chromosomes in order to resolve sexual conflict. Here we test this model using whole genome and transcriptome resequencing data in the guppy, a model for sexual selection with many Y-linked colour traits. We show that although the nascent Y chromosome encompasses nearly half of the linkage group, there has been no perceptible degradation of Y chromosome gene content or activity. Using replicate wild populations with differing levels of sexually antagonistic selection for colour, we also show that sexual selection leads to greater expansion of the non-recombining region and increased Y chromosome divergence. These results provide empirical support for longstanding models of sex chromosome catalysis, and suggest an important role for sexual selection and sexual conflict in genome evolution.

  • 24. Wright, Alison E.
    et al.
    Fumagalli, Matteo
    Cooney, Christopher R.
    Bloch, Natasha
    Vieira, Filipe G.
    Buechel, Severine D.
    Stockholm University, Faculty of Science, Department of Zoology.
    Kolm, Niclas
    Stockholm University, Faculty of Science, Department of Zoology.
    Mank, Judith E.
    Male-biased gene expression resolves sexual conflict through the evolution of sex-specific genetic architecture2018In: Evolution Letters, ISSN 2056-3744, Vol. 2, no 2, p. 52-61Article in journal (Refereed)
    Abstract [en]

    Many genes are subject to contradictory selection pressures in males and females, and balancing selection resulting from sexual conflict has the potential to substantially increase standing genetic diversity in populations and thereby act as an important force in adaptation. However, the underlying causes of sexual conflict, and the potential for resolution, remains hotly debated. Using transcriptome-resequencing data from male and female guppies, we use a novel approach, combining patterns of genetic diversity and intersexual divergence in allele frequency, to distinguish the different scenarios that give rise to sexual conflict, and how this conflict may be resolved through regulatory evolution. We show that reproductive fitness is the main source of sexual conflict, and this is resolved via the evolution of male-biased expression. Furthermore, resolution of sexual conflict produces significant differences in genetic architecture between males and females, which in turn lead to specific alleles influencing sex-specific viability. Together, our findings suggest an important role for sexual conflict in shaping broad patterns of genome diversity, and show that regulatory evolution is a rapid and efficient route to the resolution of conflict.

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