My research focuses on brain evolution and the link between variation in brain morphology and behaviour. I study this in a variety of taxa (Cichlids, Pipefishes and Seahorses, Birds, Dogs, Pinnipeds, Cetaceans, Salmonids, Poeciliids) using phylogenetic comparative analysis and laboratory experiments. For this, we have substantial laboratory facilities with room for over 4000 aquaria, mainly populated with different guppy selection lines, and six separate rooms for behavioural assays of for instance cognition, mate choice, and collective motion in small fish.
My diverse research group typically consists of 1-3 PhD students, 1-3 postdocs, and several Swedish and international masters and internship students.
Currently, most of the work in my group builds on four systems:
1. PHYLOGENETIC COMPARATIVE ANALYSES IN VERTEBRATES
We have a database with data on brain size and various aspects of life history and behaviour for over 20000 specimens from over 4500 species. We use this data to perform phylogenetic comparative analyses to test various hypotheses in a macroevolutionary framework. Currently this is mainly a collaboration with John Fitzpatrick, David Wheatcroft, Wouter van der Bijl, Andrew Iwaniuk and Masahito Tsuboi but many other important collaborators have helped in this project.
2. ARTIFICIAL SELECTION AND EXPERIMENTAL ASSAYS OF HOW BRAIN MORPHOLOGY VARIATION AFFECTS PHYSIOLOGY AND BEHAVIOUR IN THE GUPPY
We use our recently developed guppy selection lines with i) 14 % difference in brain size and ii) > 10 % difference in relative telencephalon size to perform experimental tests of several hypotheses concerning brain evolution and the link between brain morphology and physiology and behaviour. For this work, we have over 250 m2 of lab space with room for >4000 aquaria and six separate rooms for behavioural assays. This is a project with multiple collaborators, for instance Alexander Kotrschal (previously postdoc with me but now independent PI), John Fitzpatrick, David Wheatcroft, Judith Mank, Michael Jennions, Pertti Panula, Alexei Maklakov, Björn Rogell, Pavel Nemec and Neus Visa.
3. USING DOG BREEDS AS A SYSTEM FOR BRAIN AND BEHAVIOUR EVOLUTION ANALYSES
Together with collaborators Hans Temrin, Laszlo Garamszegi, Eniko Kubinyi and Adam Miklosi we study brain and behaviour evolution both within and across breeds thus using the dog breeds as a long term selection experiment.
4. ARTIFICIAL SELECTION AND EXPERIMENTAL ASSAYS OF HOW BRAIN AND BEHAVIOUR IS AFFECTED BY SELECTION ON SCHOOLING BEHAVIOUR IN THE GUPPY
We use our third type of guppy selection lines with > 15 % difference in schooling behaviour after three generations of selection. The aim here is to elucidate what changes in brain anatomy, cognition, other behaviours, life history and genetic architecture that occur when 'a guppy becomes a herring'. This is a collaboration with David Sumpter, Kristiaan Pelckmans and Judith Mank.
A selection from Stockholm University publication database
Artificial mosaic brain evolution of relative telencephalon size improves inhibitory control abilities in the guppy (Poecilia reticulata)
2022. Zegni Triki (et al.). Evolution 76 (1), 128-138Article
Mosaic brain evolution, the change in the size of separate brain regions in response to selection on cognitive performance, is an important idea in the field of cognitive evolution. However, untill now, most of the data on how separate brain regions respond to selection and their cognitive consequences stem from comparative studies. To experimentally investigate the influence of mosaic brain evolution on cognitive ability, we used male guppies artificially selected for large and small telencephalons relative to the rest of the brain. Here, we tested an important aspect of executive cognitive ability using a detour task. We found that males with larger telencephalons outperformed males with smaller telencephalons. Fish with larger telencephalons showed faster improvement in performance during detour training and were more successful in reaching the food reward without touching the transparent barrier (i.e., through correct detouring) during the test phase. Together, our findings provide the first experimental evidence showing that evolutionary enlargement of relative telencephalon size confers cognitive benefits, supporting an important role for mosaic brain evolution during cognitive evolution.
Brain morphology correlates of learning and cognitive flexibility in a fish species (Poecilia reticulata)
2022. Zegni Triki (et al.). Proceedings of the Royal Society of London. Biological Sciences 289 (1978)Article
Determining how variation in brain morphology affects cognitive abilities is important to understand inter-individual variation in cognition and, ultimately, cognitive evolution. Yet, despite many decades of research in this area, there is surprisingly little experimental data available from assays that quantify cognitive abilities and brain morphology in the same individuals. Here, we tested female guppies (Poecilia reticulata) in two tasks, colour discrimination and reversal learning, to evaluate their learning abilities and cognitive flexibility. We then estimated the size of five brain regions (telencephalon, optic tectum, hypothalamus, cerebellum and dorsal medulla), in addition to relative brain size. We found that optic tectum relative size, in relation to the rest of the brain, correlated positively with discrimination learning performance, while relative telencephalon size correlated positively with reversal learning performance. The other brain measures were not associated with performance in either task. By evaluating how fast learning occurs and how fast an animal adjusts its learning rules to changing conditions, we find support for that different brain regions have distinct functional correlations at the individual level. Importantly, telencephalon size emerges as an important neural correlate of higher executive functions such as cognitive flexibility. This is rare evidence supporting the theory that more neural tissue in key brain regions confers cognitive benefits.
Rapid mosaic brain evolution under artificial selection for relative telencephalon size in the guppy (Poecilia reticulata)
2021. Stephanie Fong (et al.). Science Advances 7 (46)Article
The mosaic brain evolution hypothesis, stating that brain regions can evolve relatively independently during cognitive evolution, is an important idea to understand how brains evolve with potential implications even for human brain evolution. Here, we provide the first experimental evidence for this hypothesis through an artificial selection experiment in the guppy (Poecilia reticulata). After four generations of selection on relative telencephalon volume (relative to brain size), we found substantial changes in telencephalon size but no changes in other regions. Further comparisons revealed that up-selected lines had larger telencephalon, while down-selected lines had smaller telencephalon than wild Trinidadian populations. Our results support that independent evolutionary changes in specific brain regions through mosaic brain evolution can be important facilitators of cognitive evolution.
The link between selection for function and human-directed play behaviour in dogs
2020. Niclas Kolm (et al.). Biology Letters 16 (9)Article
Human-directed play behaviour is a distinct behavioural feature of domestic dogs. But the role that artificial selection for contemporary dog breeds has played for human-directed play behaviour remains elusive. Here, we investigate how human-directed play behaviour has evolved in relation to the selection for different functions, considering processes of shared ancestry and gene flow among the different breeds. We use the American Kennel Club (AKC) breed group categorization to reflect the major functional differences and combine this with observational data on human-directed play behaviour for over 132 breeds across 89 352 individuals from the Swedish Dog Mentality Assessment project. Our analyses demonstrate that ancestor dogs already showed intermediate levels of human-directed play behaviour, levels that are shared with several modern breed types. Herding and Sporting breeds display higher levels of human-directed play behaviour, statistically distinguishable from Non-sporting and Toy breeds. Our results suggest that human-directed play behaviour played a role in the early domestication of dogs and that subsequent artificial selection for function has been important for contemporary variation in a behavioural phenotype mediating the social bond with humans.
Rapid evolution of coordinated and collective movement in response to artificial selection
2020. Alexander Kotrschal (et al.). Science Advances 6 (49)Article
Collective motion occurs when individuals use social interaction rules to respond to the movements and positions of their neighbors. How readily these social decisions are shaped by selection remains unknown. Through artificial selection on fish (guppies, Poecilia reticulata) for increased group polarization, we demonstrate rapid evolution in how individuals use social interaction rules. Within only three generations, groups of polarization-selected females showed a 15% increase in polarization, coupled with increased cohesiveness, compared to fish from control lines. Although lines did not differ in their physical swimming ability or exploratory behavior, polarization-selected fish adopted faster speeds, particularly in social contexts, and showed stronger alignment and attraction responses to multiple neighbors. Our results reveal the social interaction rules that change when collective behavior evolves.
Long life evolves in large-brained bird lineages
2020. Dante Jiménez-Ortega (et al.). Evolution 74 (12), 2617-2628Article
The brain is an energetically costly organ that consumes a disproportionate amount of resources. Species with larger brains relative to their body size have slower life histories, with reduced output per reproductive event and delayed development times that can be offset by increasing behavioral flexibility. The cognitive buffer hypothesis maintains that large brain size decreases extrinsic mortality due to greater behavioral flexibility, leading to a longer lifespan. Alternatively, slow life histories, and long lifespan can be a pre-adaptation for the evolution of larger brains. Here, we use phylogenetic path analysis to contrast different evolutionary scenarios and disentangle direct and indirect relationships between brain size, body size, life history, and longevity across 339 altricial and precocial bird species. Our results support both a direct causal link between brain size and lifespan, and an indirect effect via other life history traits. These results indicate that large brain size engenders longer life, as proposed by the cognitive buffer hypothesis.
Artificial selection on brain size leads to matching changes in overall number of neurons
2019. Lucie Marhounová (et al.). Evolution 73 (9), 2003-2012Article
Neurons are the basic computational units of the brain, but brain size is the predominant surrogate measure of brain functional capacity in comparative and cognitive neuroscience. This approach is based on the assumption that larger brains harbor higher numbers of neurons and their connections, and therefore have a higher information-processing capacity. However, recent studies have shown that brain mass may be less strongly correlated with neuron counts than previously thought. Till now, no experimental test has been conducted to examine the relationship between evolutionary changes in brain size and the number of brain neurons. Here, we provide such a test by comparing neuron number in artificial selection lines of female guppies (Poecilia reticulata) with >15% difference in relative brain mass and numerous previously demonstrated cognitive differences. Using the isotropic fractionator, we demonstrate that large-brained females have a higher overall number of neurons than small-brained females, but similar neuronal densities. Importantly, this difference holds also for the telencephalon, a key region for cognition. Our study provides the first direct experimental evidence that selection for brain mass leads to matching changes in number of neurons and shows that brain size evolution is intimately linked to the evolution of neuron number and cognition.
Large brains, short life: selection on brain size impacts intrinsic lifespan
2019. Alexander Kotrschal, Alberto Corral-Lopez, Niclas Kolm. Biology Letters 15 (5)Article
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.
Breakdown of brain-body allometry and the encephalization of birds and mammals
2018. Masahito Tsuboi (et al.). Nature Ecology & Evolution 2 (9), 1492-1500Article
The allometric relationship between brain and body size among vertebrates is often considered a manifestation of evolutionary constraints. However, birds and mammals have undergone remarkable encephalization, in which brain size has increased without corresponding changes in body size. Here, we explore the hypothesis that a reduction of phenotypic integration between brain and body size has facilitated encephalization in birds and mammals. Using a large dataset comprising 20,213 specimens across 4,587 species of jawed vertebrates, we show that the among-species (evolutionary) brain-body allometries are remarkably constant, both across vertebrate classes and across taxonomic levels. Birds and mammals, however, are exceptional in that their within-species (static) allometries are shallower and more variable than in other vertebrates. These patterns are consistent with the idea that birds and mammals have reduced allometric constraints that are otherwise ubiquitous across jawed vertebrates. Further exploration of ontogenetic allometries in selected taxa of birds, fishes and mammals reveals that birds and mammals have extended the period of fetal brain growth compared to fishes. Based on these findings, we propose that avian and mammalian encephalization has been contingent on increased variability in brain growth patterns.
Early neurogenomic response associated with variation in guppy female mate preference
2018. Natasha Bloch (et al.). Nature Ecology & Evolution 2 (11), 1772-1781Article
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.
Male-biased gene expression resolves sexual conflict through the evolution of sex-specific genetic architecture
2018. Alison E. Wright (et al.). Evolution Letters 2 (2), 52-61Article
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.
Brain size affects performance in a reversal-learning test
2018. Séverine D. Buechel (et al.). Proceedings of the Royal Society of London. Biological Sciences 285 (1871)Article
It has become increasingly clear that a larger brain can confer cognitive benefits. Yet not all of the numerous aspects of cognition seem to be affected by brain size. Recent evidence suggests that some more basic forms of cognition, for instance colour vision, are not influenced by brain size. We therefore hypothesize that a larger brain is especially beneficial for distinct and gradually more complex aspects of cognition. To test this hypothesis, we assessed the performance of brain size selected female guppies (Poecilia reticulata) in two distinct aspects of cognition that differ in cognitive complexity. In a standard reversal-learning test we first investigated basic learning ability with a colour discrimination test, then reversed the reward contingency to specifically test for cognitive flexibility. We found that large-brained females outperformed small-brained females in the reversed-learning part of the test but not in the colour discrimination part of the test. Large-brained individuals are hence cognitively more flexible, which probably yields fitness benefits, as they may adapt more quickly to social and/or ecological cognitive challenges. Our results also suggest that a larger brain becomes especially advantageous with increasing cognitive complexity. These findings corroborate the significance of brain size for cognitive evolution.
Convergent recombination suppression suggests role of sexual selection in guppy sex chromosome formation
2017. Alison E. Wright (et al.). Nature Communications 8Article
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.
Evolution of brain region volumes during artificial selection for relative brain size
2017. Alexander Kotrschal (et al.). Evolution 71 (12), 2942-2951Article
The vertebrate brain shows an extremely conserved layout across taxa. Still, the relative sizes of separate brain regions vary markedly between species. One interesting pattern is that larger brains seem associated with increased relative sizes only of certain brain regions, for instance telencephalon and cerebellum. Till now, the evolutionary association between separate brain regions and overall brain size is based on comparative evidence and remains experimentally untested. Here, we test the evolutionary response of brain regions to directional selection on brain size in guppies (Poecilia reticulata) selected for large and small relative brain size. In these animals, artificial selection led to a fast response in relative brain size, while body size remained unchanged. We use microcomputer tomography to investigate how the volumes of 11 main brain regions respond to selection for larger versus smaller brains. We found no differences in relative brain region volumes between large- and small-brained animals and only minor sex-specific variation. Also, selection did not change allometric scaling between brain and brain region sizes. Our results suggest that brain regions respond similarly to strong directional selection on relative brain size, which indicates that brain anatomy variation in contemporary species most likely stem from direct selection on key regions.
An efficient method for sorting and quantifying individual social traits based on group-level behaviour
2017. Alex Szorkovszky (et al.). Methods in Ecology and Evolution 8 (12), 1735-1744Article
1. In social contexts, animal behaviour is often studied in terms of group-level characteristics. One clear example of this is the collective motion of animals in decentralized structures, such as bird flocks and fish schools. A major goal of research is to identify how group-level behaviours are shaped by the traits of individuals within them. Few methods exist to make these connections. Individual assessment is often limited, forcing alternatives such as fitting agent-based models to experimental data. 2. We provide a systematic experimental method for sorting animals according to socially relevant traits, without assaying them or even tagging them individually. Instead, they are repeatedly subjected to behavioural assays in groups, between which the group memberships are rearranged, in order to test the effect of many different combinations of individuals on a group-level property or feature. We analyse this method using a general model for the group feature, and simulate a variety of specific cases to track how individuals are sorted in each case. 3. We find that in the case where the members of a group contribute equally to the group feature, the sorting procedure increases the between-group behavioural variation well above what is expected for groups randomly sampled from a population. For a wide class of group feature models, the individual phenotypes are efficiently sorted across the groups and thus become available for further analysis on how individual properties affect group behaviour. We also show that the experimental data can be used to estimate the individual-level repeatability of the underlying traits. 4. Our method allows experimenters to find repeatable variation in social behaviours that cannot be assessed in solitary individuals. Furthermore, experiments in animal behaviour often focus on comparisons between groups randomly sampled from a population. Increasing the behavioural variation between groups increases statistical power for testing whether a group feature is related to other properties of groups or to their phenotypic composition. Sorting according to socially relevant traits is also beneficial in artificial selection experiments, and for testing correlations with other traits. Overall, the method provides a useful tool to study how individual properties influence social behaviour.
Female brain size affects the assessment of male attractiveness during mate choice
2017. Alberto Corral-López (et al.). Science Advances 3 (3)Article
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.
Artificial selection on male genitalia length alters female brain size
2016. Séverine D. Buechel (et al.). Proceedings of the Royal Society of London. Biological Sciences 283 (1843)Article
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.
Selection for brain size impairs innate, but not adaptive immune responses
2016. Alexander Kotrschal, Niclas Kolm, Dustin J. Penn. Proceedings of the Royal Society of London. Biological Sciences 283 (1826)Article
Both the brain and the imnume system are energetically demanding organs, and when natural selection favours increased investment into one, then the size or performance of the other should be reduced. While comparative analyses have attempted to test this potential evolutionary trade-off, the results remain inconclusive. To test this hypothesis, we compared the tissue graft rejection (an assay for measuring innate and acquired immune responses) in guppies (Poecilia reticulata) artificially selected for large and small relative brain size. Individual scales were transplanted between pairs of fish, creating reciprocal allografts, and the rejection reaction was scored over 8 days (before acquired immunity develops). Acquired immune responses were tested two weeks later, when the same pairs of fish received a second set of allografts and were scored again. Compared with large-brained animals, small-brained animals of both sexes mounted a significantly stronger rejection response to the first allograft. The rejection response to the second set of allografts did not differ between large- and small-brained fish. Our results show that selection for large brain size reduced innate immune responses to an allograft, which supports the hypothesis that there is a selective trade-off between investing into brain size and innate immunity.
Why direct effects of predation complicate the social brain hypothesis And how incorporation of explicit proximate behavioral mechanisms might help
2016. Wouter van der Bijl, Niclas Kolm. Bioessays 38 (6), 568-577Article
A growing number of studies have found that large brains may help animals survive by avoiding predation. These studies provide an alternative explanation for existing correlative evidence for one of the dominant hypotheses regarding the evolution of brain size in animals, the social brain hypothesis (SBH). The SBH proposes that social complexity is a major evolutionary driver of large brains. However, if predation both directly selects for large brains and higher levels of sociality, correlations between sociality and brain size may be spurious. We argue that tests of the SBH should take direct effects of predation into account, either by explicitly including them in comparative analyses or by pin-pointing the brain-behavior-fitness pathway through which the SBH operates. Existing data and theory on social behavior can then be used to identify precise candidate mechanisms and formulate new testable predictions.
Evolution of brain-body allometry in Lake Tanganyika cichlids
2016. Masahito Tsuboi (et al.). Evolution 70 (7), 1559-1568Article
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.
Brain size affects female but not male survival under predation threat
2015. Alexander Kotrschal (et al.). Ecology Letters 18 (7), 646-652Article
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.
Brain size affects the behavioural response to predators in female guppies (Poecilia reticulata)
2015. Wouter van der Bijl (et al.). Proceedings of the Royal Society of London. Biological Sciences 282 (1812), 116-124Article
Large brains are thought to result from selection for cognitive benefits, but how enhanced cognition leads to increased fitness remains poorly understood. One explanation is that increased cognitive ability results in improved monitoring and assessment of predator threats. Here, we use male and female guppies (Poecilia reticulata), artificially selected for large and small brain size, to provide an experimental evaluation of this hypothesis. We examined their behavioural response as singletons, pairs or shoals of four towards a model predator. Large-brained females, but not males, spent less time performing predator inspections, an inherently risky behaviour. Video analysis revealed that large-brained females were further away from the model predator when in pairs but that they habituated quickly towards the model when in shoals of four. Males stayed further away from the predator model than females but again we found no brain size effect in males. We conclude that differences in brain size affect the female predator response. Large-brained females might be able to assess risk better or need less sensory information to reach an accurate conclusion. Our results provide experimental support for the general idea that predation pressure is likely to be important for the evolution of brain size in prey species.
Expression change in Angiopoietin-1 underlies change in relative brain size in fish
2015. Yu-Chia Chen (et al.). Proceedings of the Royal Society of London. Biological Sciences 282 (1810)Article
Brain size varies substantially across the animal kingdom and is often associated with cognitive ability; however, the genetic architecture underpinning natural variation in these key traits is virtually unknown. In order to identify the genetic architecture and loci underlying variation in brain size, we analysed both coding sequence and expression for all the loci expressed in the telencephalon in replicate populations of guppies (Poecilia reticulata) artificially selected for large and small relative brain size. A single gene, Angiopoietin-1 (Ang-1), a regulator of angiogenesis and suspected driver of neural development, was differentially expressed between large-and small-brain populations. Zebra fish (Danio rerio) morphants showed that mild knock down of Ang-1 produces a small-brained phenotype that could be rescued with Ang-1 mRNA. Translation inhibition of Ang-1 resulted in smaller brains in larvae and increased expression of Notch-1, which regulates differentiation of neural stem cells. In situ analysis of newborn large-and small-brained guppies revealed matching expression patterns of Ang-1 and Notch-1 to those observed in zebrafish larvae. Taken together, our results suggest that the genetic architecture affecting brain size in our population may be surprisingly simple, and Ang-1 may be a potentially important locus in the evolution of vertebrate brain size and cognitive ability.
The effect of brain size evolution on feeding propensity, digestive efficiency, and juvenile growth
2015. Alexander Kotrschal (et al.). Evolution 69 (11), 3013-3020Article
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.
Artificial selection on relative brain size reveals a positive genetic correlation between brain size and proactive personality in the guppy
2014. Alexander Kotrschal (et al.). Evolution 68 (4), 1139-1149Article
Animal personalities range from individuals that are shy, cautious, and easily stressed (a reactive personality type) to individuals that are bold, innovative, and quick to learn novel tasks, but also prone to routine formation (a proactive personality type). Although personality differences should have important consequences for fitness, their underlying mechanisms remain poorly understood. Here, we investigated how genetic variation in brain size affects personality. We put selection lines of large- and small-brained guppies (Poecilia reticulata), with known differences in cognitive ability, through three standard personality assays. First, we found that large-brained animals were faster to habituate to, and more exploratory in, open field tests. Large-brained females were also bolder. Second, large-brained animals excreted less cortisol in a stressful situation (confinement). Third, large-brained animals were slower to feed from a novel food source, which we interpret as being caused by reduced behavioral flexibility rather than lack of innovation in the large-brained lines. Overall, the results point toward a more proactive personality type in large-brained animals. Thus, this study provides the first experimental evidence linking brain size and personality, an interaction that may affect important fitness-related aspects of ecology such as dispersal and niche exploration.
Artificial selection on relative brain size in the guppy reveals costs and benefits of evolving a larger brain
2013. Alexander Kotrschal (et al.). Current Biology 23 (2), 168-171Article
The large variation in brain size that exists in the animal kingdom has been suggested to have evolved through the balance between selective advantages of greater cognitive ability and the prohibitively high energy demands of a larger brain (the "expensive-tissue hypothesis" ). Despite over a century of research on the evolution of brain size, empirical support for the trade-off between cognitive ability and energetic costs is based exclusively on correlative evidence , and the theory remains controversial [3, 4]. Here we provide experimental evidence for costs and benefits of increased brain size. We used artificial selection for large and small brain size relative to body size in a live-bearing fish, the guppy (Poecilia reticulata), and found that relative brain size evolved rapidly in response to divergent selection in both sexes. Large-brained females outperformed small-brained females in a numerical learning assay designed to test cognitive ability. Moreover, large-brained lines, especially males, developed smaller guts, as predicted by the expensive-tissue hypothesis , and produced fewer offspring. We propose that the evolution of brain size is mediated by a functional trade-off between increased cognitive ability and reproductive performance and discuss the implications of these findings for vertebrate brain evolution.
Diversification of a Food-Mimicking Male Ornament via Sensory Drive
2012. Niclas Kolm (et al.). Current Biology 22 (15), 1440-1443Article
The evolutionary divergence of sexual signals is often important during the formation of new animal species, but our understanding of the origin of signal diversity is limited [1, 2]. Sensory drive, the optimization of communication signal efficiency through matching to the local environment, has been highlighted as a potential promoter of diversification and speciation . The swordtail characin (Corynopoma riisei) is a tropical fish in which males display a flag-like ornament that elicits female foraging behavior during courtship. We show that the shape of the male ornament covaries with female diet across natural populations. More specifically, natural populations in which the female diet is more dominated by ants exhibit male ornaments more similar to the shape of an ant. Feeding experiments confirm that females habituated to a diet of ants prefer to bite at male ornaments from populations with a diet more dominated by ants. Our results show that the male ornament functions as a "fishing lure" that is diversifying in shape to match local variation in female search images employed during foraging. This direct link between variation in female feeding ecology and the evolutionary diversification of male sexual ornaments suggests that sensory drive may be a common engine of signal divergence.
Male Contest Competition And The Coevolution Of Weaponry And Testes In Pinnipeds
2012. J. L. Fitzpatrick (et al.). Evolution 66 (11), 3595-3604Article
Male reproductive success is influenced by competitive interactions during precopulatory and postcopulatory selective episodes. Consequently, males can gain reproductive advantages during precopulatory contest competition by investing in weaponry and during postcopulatory sperm competition by investing in ejaculates. However, recent theory predicts male expenditure on weaponry and ejaculates should be subject to a trade-off, and should vary under increasing risk and intensity of sperm competition. Here, we provide the first comparative analysis of the prediction that expenditure on weaponry should be negatively associated with expenditure on testes mass. Specifically, we assess how sexual selection influences the evolution of primary and secondary sexual traits among pinnipeds (seals, sea lions, and walruses). Using recently developed comparative methods, we demonstrate that sexual selection promotes rapid divergence in body mass, sexual size dimorphism (SSD), and genital morphology. We then show that genital length appears to be positively associated with the strength of postcopulatory sexual selection. However, subsequent analyses reveal that both genital length and testes mass are negatively associated with investment in precopulatory weaponry. Thus, our results are congruent with recent theoretical predictions of contest-based sperm competition models. We discuss the possible role of trade-offs and allometry in influencing patterns of reproductive trait evolution in pinnipeds.
Female promiscuity promotes the evolution of faster sperm in cichlid fishes
2009. John L. Fitzpatrick (et al.). Proceedings of the National Academy of Sciences of the United States of America 106 (4), 1128-1132Article
Sperm competition, the contest among ejaculates from rival males to fertilize ova of a female, is a common and powerful evolutionary force influencing ejaculate traits. During competitive interactions between ejaculates, longer and faster spermatozoa are expected to have an edge; however, to date, there has been mixed support for this key prediction from sperm competition theory. Here, we use the spectacular radiation of cichlid fishes from Lake Tanganyika to examine sperm characteristics in 29 closely related species. We provide phylogenetically robust evidence that species experiencing greater levels of sperm competition have faster-swimming sperm. We also show that sperm competition selects for increases in the number, size, and longevity of spermatozoa in the ejaculate of a male, and, contrary to expectations from theory, we find no evidence of trade-offs among sperm traits in an interspecific analysis. Also, sperm swimming speed is positively correlated with sperm length among, but not within, species. These different responses to sperm competition at intra-and interspecific levels provide a simple, powerful explanation for equivocal results from previous studies. Using phylogenetic analyses, we also reconstructed the probable evolutionary route of trait evolution in this taxon, and show that, in response to increases in the magnitude of sperm competition, the evolution of sperm traits in this clade began with the evolution of faster (thus, more competitive) sperm.
Social fishes and single mothers: brain evolution in African cichlids
2009. Alejandro Gonzalez-Voyer, Svante Winberg, Niclas Kolm. Proceedings of the Royal Society of London. Biological Sciences 276 (1654), 161-167Article
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.
Sexual selection determines parental care patterns in cichlid fishes
2008. Alejandro Gonzalez-Voyer, John L. Fitzpatrick, Niclas Kolm. Evolution 62 (8), 2015-2026Article
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.
Species diversity can drive speciation
2005. B. C. Emerson, Niclas Kolm. Nature 434 (7036), 1015-1017Article
A fundamental question in evolutionary ecology and conservation biology is: why do some areas contain greater species diversity than others? Island biogeographic theory has identified the roles of immigration and extinction in relation to area size and proximity to source areas(1,2), and the role of speciation is also recognized as an important factor(3-6). However, one as yet unexplored possibility is that species diversity itself might help to promote speciation, and indeed the central tenets of island biogeographic theory support such a prediction. Here we use data for plants and arthropods of the volcanic archipelagos of the Canary and Hawaiian Islands to address whether there is a positive relationship between species diversity and rate of diversification. Our index of diversification for each island is the proportion of species that are endemic, and we test our prediction that this increases with increasing species number. We show that even after controlling for several important physical features of islands, diversification is strongly related to species number.
Females produce larger eggs for large males in a paternal mouthbrooding fish
2001. Niclas Kolm. Proceedings of the Royal Society of London. Biological Sciences 268 (1482), 2229-2234Article
When individuals receive different returns from their reproductive investment dependent on mate quality, they are expected to invest more when breeding with higher quality mates. A number of studies over the past decade have shown that females may alter their reproductive effort depending on the quality/attractiveness of their mate. However, to date, despite extensive work on parental investment, such a differential allocation has not been demonstrated in fish. Indeed, so far only two studies from any taxon have suggested that females alter the quality of individual offspring according to the quality/attractiveness of their mate. The banggai cardinal fish is an obligate paternal mouth brooder where females lay few large eggs. It has previously been shown that male size determines clutch weight irrespective of female size in this species. In this study, I investigated whether females perform more courtship displays towards larger males and whether females allocate their reproductive effort depending on the size of their mate by experimentally assigning females to either large or small males. I found that females displayed more towards larger males, thereby suggesting a female preference for larger males. Further, females produced heavier eggs and heavier clutches but not more eggs when paired with large males. My experiments show that females in this species adjust their offspring weight and, thus, presumably offspring quality according to the size of their mate.