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  • 1.
    Gonzalez-Voyer, Alejandro
    et al.
    Uppsala universitet, Institutionen för ekologi och evolution.
    Fitzpatrick, John L.
    Kolm, Niclas
    Uppsala universitet, Institutionen för ekologi och evolution.
    Sexual selection determines parental care patterns in cichlid fishes2008In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 62, no 8, p. 2015-2026Article in journal (Refereed)
    Abstract [en]

    Despite a massive research effort, our understanding of why, in most vertebrates, males compete for mates and females care for offspring remains incomplete. Two alternative hypotheses have been proposed to explain the direction of causality between parental care and sexual selection. Traditionally, sexual selection has been explained as a consequence of relative parental investment, where the sex investing less will compete for the sex investing more. However, a more recent model suggests that parental care patterns result from sexual selection acting on one sex favoring mating competition and lower parental investment. Using species-level comparative analyses on Tanganyikan cichlid fishes we tested these alternative hypotheses employing a proxy of sexual selection based on mating system, sexual dichromatism, and dimorphism data. First, while controlling for female reproductive investment, we found that species with intense sexual selection were associated with female-only care whereas species with moderate sexual selection were associated with biparental care. Second, using contingency analyses, we found that, contrary to the traditional view, evolutionary changes in parental care type are dependent on the intensity of sexual selection. Hence, our results support the hypothesis that sexual selection determines parental care patterns in Tanganyikan cichlid fishes.

  • 2.
    Gonzalez-Voyer, Alejandro
    et al.
    Uppsala universitet, Zooekologi.
    Kolm, Niclas
    Uppsala universitet, Zooekologi.
    Rates of phenotypic evolution of ecological characters and sexual traits during the Tanganyikan cichlid adaptive radiation2011In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 24, no 11, p. 2378-2388Article in journal (Refereed)
    Abstract [en]

    Theory suggests that sexual traits evolve faster than ecological characters. However, characteristics of a species niche may also influence evolution of sexual traits. Hence, a pending question is whether ecological characters and sexual traits present similar tempo and mode of evolution during periods of rapid ecological divergence, such as adaptive radiation. Here, we use recently developed phylogenetic comparative methods to analyse the temporal dynamics of evolution for ecological and sexual traits in Tanganyikan cichlids. Our results indicate that whereas disparity in ecological characters was concentrated early in the radiation, disparity in sexual traits remained high throughout the radiation. Thus, closely related Tanganyikan cichlids presented higher disparity in sexual traits than ecological characters. Sexual traits were also under stronger selection than ecological characters. In sum, our results suggest that ecological characters and sexual traits present distinct evolutionary patterns, and that sexual traits can evolve faster than ecological characters, even during adaptive radiation.

  • 3.
    Gonzalez-Voyer, Alejandro
    et al.
    Consejo Superior de Investigación Científica (CSIC), Spain; Uppsala University, Sweden.
    Kolm, Niclas
    Uppsala University, Sweden.
    Sex, Ecology and the Brain: Evolutionary Correlates of Brain Structure Volumes in Tanganyikan Cichlids2010In: PLOS ONE, E-ISSN 1932-6203, Vol. 5, no 12, article id e14355Article in journal (Refereed)
    Abstract [en]

    Analyses of the macroevolutionary correlates of brain structure volumes allow pinpointing of selective pressures influencing specific structures. Here we use a multiple regression framework, including phylogenetic information, to analyze brain structure evolution in 43 Tanganyikan cichlid species. We analyzed the effect of ecological and sexually selected traits for species averages, the effect of ecological traits for each sex separately and the influence of sexual selection on structure dimorphism. Our results indicate that both ecological and sexually selected traits have influenced brain structure evolution. The patterns observed in males and females generally followed those observed at the species level. Interestingly, our results suggest that strong sexual selection is associated with reduced structure volumes, since all correlations between sexually selected traits and structure volumes were negative and the only statistically significant association between sexual selection and structure dimorphism was also negative. Finally, we previously found that monoparental female care was associated with increased brain size. However, here cerebellum and hypothalamus volumes, after controlling for brain size, associated negatively with female-only care. Thus, in accord with the mosaic model of brain evolution, brain structure volumes may not respond proportionately to changes in brain size. Indeed selection favoring larger brains can simultaneously lead to a reduction in relative structure volumes.

  • 4.
    Gonzalez-Voyer, Alejandro
    et al.
    Uppsala universitet, Zooekologi.
    Winberg, Svante
    Uppsala universitet, Fysiologi.
    Kolm, Niclas
    Uppsala universitet, Zooekologi.
    Brain structure evolution in a basal vertebrate clade: evidence from phylogenetic comparative analysis of cichlid fishes2009In: BMC Evolutionary Biology, E-ISSN 1471-2148, Vol. 9, p. 238-Article in journal (Refereed)
    Abstract [en]

     Background: The vertebrate brain is composed of several interconnected, functionally distinct structures and much debate has surrounded the basic question of how these structures evolve. On the one hand, according to the 'mosaic evolution hypothesis', because of the elevated metabolic cost of brain tissue, selection is expected to target specific structures mediating the cognitive abilities which are being favored. On the other hand, the 'concerted evolution hypothesis' argues that developmental constraints limit such mosaic evolution and instead the size of the entire brain varies in response to selection on any of its constituent parts. To date, analyses of these hypotheses of brain evolution have been limited to mammals and birds; excluding Actinopterygii, the basal and most diverse class of vertebrates. Using a combination of recently developed phylogenetic multivariate allometry analyses and comparative methods that can identify distinct rates of evolution, even in highly correlated traits, we studied brain structure evolution in a highly variable clade of ray-finned fishes; the Tanganyikan cichlids.

    Results: Total brain size explained 86% of the variance in brain structure volume in cichlids, a lower proportion than what has previously been reported for mammals. Brain structures showed variation in pair-wise allometry suggesting some degree of independence in evolutionary changes in size. This result is supported by variation among structures on the strength of their loadings on the principal size axis of the allometric analysis. The rate of evolution analyses generally supported the results of the multivariate allometry analyses, showing variation among several structures in their evolutionary patterns. The olfactory bulbs and hypothalamus were found to evolve faster than other structures while the dorsal medulla presented the slowest evolutionary rate.

    Conclusion: Our results favor a mosaic model of brain evolution, as certain structures are evolving in a modular fashion, with a small but non-negligible influence of concerted evolution in cichlid fishes. Interestingly, one of the structures presenting distinct evolutionary patterns within cichlids, the olfactory bulbs, has also been shown to evolve differently from other structures in mammals. Hence, our results for a basal vertebrate clade also point towards a conserved developmental plan for all vertebrates.

  • 5.
    Gonzalez-Voyer, Alejandro
    et al.
    Uppsala universitet, Zooekologi.
    Winberg, Svante
    Uppsala universitet, Fysiologi.
    Kolm, Niclas
    Uppsala universitet, Zooekologi.
    Distinct Evolutionary Patterns of Brain and Body Size During Adaptive Radiation2009In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 63, no 9, p. 2266-2274Article in journal (Refereed)
    Abstract [en]

    Morphological traits are often genetically and/or phenotypically correlated with each other and such covariation can have an important influence on the evolution of individual traits. The strong positive relationship between brain size and body size in vertebrates has attracted a lot of interest, and much debate has surrounded the study of the factors responsible for the allometric relationship between these two traits. Here, we use comparative analyses of the Tanganyikan cichlid adaptive radiation to investigate the patterns of evolution for brain size and body size separately. We found that body size exhibited recent bursts of rapid evolution, a pattern that is consistent with divergence linked to ecological specialization. Brain weight on the other hand, showed no bursts of divergence but rather evolved in a gradual manner. Our results thus show that even highly genetically correlated traits can present markedly different patterns of evolution, hence interpreting patterns of evolution of traits from correlations in extant taxa can be misleading. Furthermore, our results suggest, contrary to expectations from theory, that brain size does not play a key role during adaptive radiation.

  • 6.
    Gonzalez-Voyer, Alejandro
    et al.
    Uppsala universitet, Zooekologi.
    Winberg, Svante
    Uppsala universitet, Fysiologi.
    Kolm, Niclas
    Uppsala universitet, Zooekologi.
    Social fishes and single mothers: brain evolution in African cichlids2009In: Proceedings of the Royal Society of London. Biological Sciences, ISSN 0962-8452, E-ISSN 1471-2954, Vol. 276, no 1654, p. 161-167Article in journal (Refereed)
    Abstract [en]

    As with any organ, differences in brain size-after adequate control of allometry-are assumed to be a response to selection. With over 200 species and an astonishing diversity in niche preferences and social organization, Tanganyikan cichlids present an excellent opportunity to study brain evolution. We used phylogenetic comparative analyses of sexed adults from 39 Tanganyikan cichlid species in a multiple regression framework to investigate the influence of ecology, sexual selection and parental care patterns on whole brain size, as well as to analyse sex-specific effects. First, using species-specific measures, we analysed the influence of diet, habitat, form of care (mouthbrooding or substrate guarding), care type (biparental or female only) and intensity of sexual selection on brain size, while controlling for body size. Then, we repeated the analyses for male and female brain size separately. Type of diet and care type were significantly correlated with whole brain size. Sex-specific analyses showed that female brain size correlated significantly with care type while male brain size was uncorrelated with care type. Our results suggest that more complex social interactions associated with diet select for larger brains and further that the burden of uniparental care exerts high cognitive demands on females.

  • 7.
    Kolm, Niclas
    et al.
    Uppsala universitet, Zooekologi.
    Gonzalez-Voyer, Alejandro
    Uppsala universitet, Zooekologi.
    Brelin, Daniel
    Uppsala universitet, Fysiologi.
    Winberg, Svante
    Uppsala universitet, Fysiologi.
    Evidence for small scale variation in the vertebrate brain: mating strategy and sex affect brain size and structure in wild brown trout (Salmo trutta)2009In: Journal of Evolutionary Biology, ISSN 1010-061X, E-ISSN 1420-9101, Vol. 22, no 12, p. 2524-2531Article in journal (Refereed)
    Abstract [en]

    The basis for our knowledge of brain evolution in vertebrates rests heavily on empirical evidence from comparative studies at the species level. However, little is still known about the natural levels of variation and the evolutionary causes of differences in brain size and brain structure within-species, even though selection at this level is an important initial generator of macroevolutionary patterns across species. Here, we examine how early life-history decisions and sex are related to brain size and brain structure in wild populations using the existing natural variation in mating strategies among wild brown trout (Salmo trutta). By comparing the brains of precocious fish that remain in the river and sexually mature at a small size with those of migratory fish that migrate to the sea and sexually mature at a much larger size, we show, for the first time in any vertebrate, strong differences in relative brain size and brain structure across mating strategies. Precocious fish have larger brain size (when controlling for body size) but migratory fish have a larger cerebellum, the structure in charge of motor coordination. Moreover, we demonstrate sex-specific differences in brain structure as female precocious fish have a larger brain than male precocious fish while males of both strategies have a larger telencephalon, the cognitive control centre, than females. The differences in brain size and structure across mating strategies and sexes thus suggest the possibility for fine scale adaptive evolution of the vertebrate brain in relation to different life histories.

  • 8.
    Maklakov, Alexei
    et al.
    Uppsala Universitet.
    Immler, Simone
    Uppsala Universitet.
    Gonzalez-Voyer, Alejandro
    Rönn, Johanna
    Uppsala universitet.
    Kolm, Niclas
    Brains and the city: big-brained passerine birds succeed in urban environments2011In: Biology Letters, ISSN 1744-9561, E-ISSN 1744-957X, Vol. 7, no 5, p. 730-732Article in journal (Refereed)
    Abstract [en]

    Urban regions are among the most human-altered environments on Earth and they are poised for rapid expansion following population growth and migration. Identifying the biological traits that determine which species are likely to succeed in urbanized habitats is important for predicting global trends in biodiversity. We provide the first evidence for the intuitive yet untested hypothesis that relative brain size is a key factor predisposing animals to successful establishment in cities. We apply phylogenetic mixed modelling in a Bayesian framework to show that passerine species that succeed in colonizing at least one of 12 European cities are more likely to belong to big-brained lineages than species avoiding these urban areas. These data support findings linking relative brain size with the ability to persist in novel and changing environments in vertebrate populations, and have important implications for our understanding of recent trends in biodiversity.

  • 9.
    Schäpers, Alexander
    et al.
    Stockholm University, Faculty of Science, Department of Zoology, Animal Ecology.
    Nylin, Sören
    Stockholm University, Faculty of Science, Department of Zoology, Animal Ecology.
    Gonzalez-Voyer, Alejandro
    Stockholm University, Faculty of Science, Department of Zoology, Ethology.
    Wang, Houshuai
    Wahlberg, Niklas
    Janz, Niklas
    Stockholm University, Faculty of Science, Department of Zoology, Animal Ecology.
    Clutch size and host use in butterflies - and how to measure diet breadthManuscript (preprint) (Other academic)
    Abstract [en]

    The utilization of host plants is a central aspect of herbivorous insect life-history and known to promote processes of diversification in this group. In species that aggregate their eggs, female selection of a suitable egg-laying site is especially important, since a large proportion of the realized fitness will depend on few oviposition events. A cluster of larvae also requires a large resource to complete development and thus resource size may further limit the range of suitable hosts. We investigated whether there is a relationship between clutch size and diet breadth for 206 nymphalid butterfly species, using phylogenetic comparative methods. Results were consistent across several taxonomic and phylogenetic diet breadth measures, suggesting that some taxonomic measures may be as good approximations as the more cumbersome estimates based on phylogenetic distance. Treating diet breadth and clutch size as continuous data indicated no relationship between the traits, while categorizing them into binary form showed that they evolve in a correlated fashion. The discordance between analyses indicated that clutch size may be constrained among extreme generalists, as polyphagous clutch layers were rare. We found clutch-laying to be a relatively conserved trait in the phylogeny and less flexible than variation in degree of host plant specialization. Host plant growth form did not influence the clutch size diet breath relationship, but was weakly correlated with both factors. We discuss the general role of conservative life-history traits, such as clutch size, for the evolutionary dynamics of more labile traits such as diet breadth among phytophagous insects.

  • 10.
    Sowersby, Will
    et al.
    Stockholm University, Faculty of Science, Department of Zoology. Osaka City University, Japan.
    Eckerström-Liedholm, Simon
    Stockholm University, Faculty of Science, Department of Zoology. Wild Animal Initiative, USA.
    Kotrschal, Alexander
    Stockholm University, Faculty of Science, Department of Zoology. Wageningen University, Netherlands.
    Näslund, Joacim
    Stockholm University, Faculty of Science, Department of Zoology. Swedish University of Agricultural Sciences, Sweden.
    Rowiński, Piotr
    Stockholm University, Faculty of Science, Department of Zoology.
    Gonzalez-Voyer, Alejandro
    Stockholm University, Faculty of Science, Department of Zoology. Universidad Nacional Autónoma de México, Mexico.
    Rogell, Björn
    Stockholm University, Faculty of Science, Department of Zoology. Swedish University of Agricultural Sciences, Sweden.
    Fast life-histories are associated with larger brain size in killifishes2021In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 75, no 9, p. 2286-2298Article in journal (Refereed)
    Abstract [en]

    The high energetic demands associated with the vertebrate brain are proposed to result in a trade-off between the pace of life-history and relative brain size. However, because both life-history and brain size also have a strong relationship with body size, any associations between the pace of life-history and relative brain size may be confounded by coevolution with body size. Studies on systems where contrasts in the pace of life-history occur without concordant contrasts in body size could therefore add to our understanding of the potential coevolution between relative brain size and life-history. Using one such system - 21 species of killifish - we employed a common garden design across two ontogenetic stages to investigate the association between relative brain size and the pace of life-history. Contrary to predictions, we found that relative brain size was larger in adult fast-living killifishes, compared to slow-living species. Although we found no differences in relative brain size between juvenile killifishes. Our results suggest that fast- and slow-living killifishes do not exhibit the predicted trade-off between brain size and life-history. Instead, fast and slow-living killifishes could differ in the ontogenetic timing of somatic versus neural growth or inhabit environments that differ considerably in cognitive demands.

  • 11.
    Sowersby, Will
    et al.
    Stockholm University, Faculty of Science, Department of Zoology. Osaka City University, Japan.
    Eckerström-Liedholm, Simon
    Stockholm University, Faculty of Science, Department of Zoology. Wild Animal Initiative, USA.
    Rowiński, Piotr K.
    Stockholm University, Faculty of Science, Department of Zoology.
    Balogh, Julia
    Stockholm University, Faculty of Science, Department of Zoology.
    Eiler, Stefan
    Stockholm University, Faculty of Science, Department of Zoology.
    Upstone, Joseph D.
    Stockholm University, Faculty of Science, Department of Zoology.
    Gonzalez-Voyer, Alejandro
    Stockholm University, Faculty of Science, Department of Zoology. Universidad Nacional Autónoma de México, Mexico.
    Rogell, Björn
    Stockholm University, Faculty of Science, Department of Zoology. Swedish University of Agricultural Sciences, Sweden.
    The relative effects of pace of life-history and habitat characteristics on the evolution of sexual ornaments: A comparative assessment2022In: Evolution, ISSN 0014-3820, E-ISSN 1558-5646, Vol. 76, no 1, p. 114-127Article in journal (Refereed)
    Abstract [en]

    Selection may favor greater investment into sexual ornaments when opportunities for future reproduction are limited, for example, under high adult mortality. However, predation, a key driver of mortality, typically selects against elaborate sexual ornaments. Here, we examine the evolution of sexual ornaments in killifishes, which have marked contrasts in life-history strategy among species and inhabit environments that differ in accessibility to aquatic predators. We first assessed if the size of sexual ornaments (unpaired fins) influenced swimming performance. Second, we investigated whether the evolution of larger ornamental fins is driven primarily by the pace of life-history (investment into current vs. future reproduction) or habitat type (a proxy for predation risk). We found that larger fins negatively affected swimming performance. Further, males from species inhabiting ephemeral habitats, with lower predation risk, had larger fins and greater sexual dimorphism in fin size, compared to males from more accessible permanent habitats. We show that enlarged ornamental fins, which impair locomotion, evolve more frequently in environments that are less accessible to predators, without clear associations to life-history strategy. Our results provide a rare link between the evolution of sexual ornaments, effects on locomotion performance, and natural selection on ornament size potentially through habitat differences in predation risk. 

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