Social fishes and single mothers: brain evolution in African cichlids

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.     

Neuroecology of cartilaginous fishes: the functional implications of brain scaling

It is a widely accepted view that neural development can reflect morphological adaptations and sensory specializations. The aim of this review is to give a broad overview of the current status of brain data available for cartilaginous fishes and examine how perspectives on allometric scaling of brain size across this group of fishes has changed within the last 50 years with the addition of new data and more rigorous statistical analyses. The current knowledge of neuroanatomy in cartilaginous fishes is reviewed and data on brain size (encephalization, n = 151) and interspecific variation in brain organization (n = 84) has been explored to ascertain scaling relationships across this clade. It is determined whether similar patterns of brain organization, termed cerebrotypes, exist in species that share certain lifestyle characteristics. Clear patterns of brain organization exist across cartilaginous fishes, irrespective of phylogenetic grouping and, although this study was not a functional analysis, it provides further evidence that chondrichthyan brain structures might have developed in conjunction with specific behaviours or enhanced cognitive capabilities. Larger brains, with well-developed telencephala and large, highly foliated cerebella are reported in species that occupy complex reef or oceanic habitats, potentially identifying a reef-associated cerebrotype. In contrast, benthic and benthopelagic demersal species comprise the group with the smallest brains, with a relatively reduced telencephalon and a smooth cerebellar corpus. There is also evidence herein of a bathyal cerebrotype; deep-sea benthopelagic sharks possess relatively small brains and show a clear relative hypertrophy of the medulla oblongata. Despite the patterns observed and documented, significant gaps in the literature have been highlighted. Brain mass data are only currently available on c. 16% of all chondrichthyan species, and only 8% of species have data available on their brain organization, with far less on subsections of major brain areas that receive distinct sensory input. The interspecific variability in brain organization further stresses the importance of performing functional studies on a greater range of species. Only an expansive data set, comprised of species that span a variety of habitats and taxonomic groups, with widely disparate behavioural repertoires, combined with further functional analyses, will help shed light on the extent to which chondrichthyan brains have evolved as a consequence of behaviour, habitat and lifestyle in addition to phylogeny.     

Adaptation of brain regions to habitat complexity: a comparative analysis in bats (Chiroptera)

Vertebrate brains are organized in modules which process information from sensory inputs selectively. Therefore they are probably under different evolutionary pressures. We investigated the impact of environmental influences on specific brain centres in bats. We showed in a phylogenetically independent contrast analysis that the wing area of a species corrected for body size correlated with estimates of habitat complexity. We subsequently compared wing area, as an indirect measure of habitat complexity, with the size of regions associated with hearing, olfaction and spatial memory, while controlling for phylogeny and body mass. The inferior colliculi, the largest sub-cortical auditory centre, showed a strong positive correlation with wing area in echolocating bats. The size of the main olfactory bulb did not increase with wing area, suggesting that the need for olfaction may not increase during the localization of food and orientation in denser habitat. As expected, a larger wing area was linked to a larger hippocampus in all bats. Our results suggest that morphological adaptations related to flight and neuronal capabilities as reflected by the sizes of brain regions coevolved under similar ecological pressures. Thus, habitat complexity presumably influenced and shaped sensory abilities in this mammalian order independently of each other.     

Aggression and welfare in a common aquarium fish, the Midas cichlid

Many species of fishes are aggressive when placed in small aquaria. Aggression can negatively affect the welfare of those individuals toward whom it is directed. Animals may behave aggressively in order to defend resources such as food, shelter, mates, and offspring. The decision to defend depends on the distribution of resources and on ecological factors such as number of competitors, amount of available space, and amount of habitat complexity. This study tested the effects of these factors on aggression in a common aquarium fish, the Midas cichlid (Amphilophus citrinellus). The study found that time spent behaving aggressively was not associated with small-scale differences in group size or available space. Aggression was significantly lower in a large aquarium with a complex habitat. Aquaria of sizes typically used in the companion animal (pet) hobby did not provide optimal welfare for cichlids housed with aggressive conspecifics. The public should be aware that this and similar species require larger aquaria with complex habitat, which elicit more natural behavior.     

Aggression and Welfare in a Common Aquarium Fish,the Midas Cichlid

Many species of fishes are aggressive when placed in small aquaria. Aggression can negatively affect the welfare of those individuals toward whom it is directed. Animals may behave aggressively in order to defend resources such as food, shelter, mates, and offspring. The decision to defend depends on the distribution of resources and on ecological factors such as number of competitors, amount of available space, and amount of habitat complexity. This study tested the effects of these factors on aggression in a common aquarium fish, the Midas cichlid (Amphilophus citrinellus). The study found that time spent behaving aggressively was not associated with small-scale differences in group size or available space. Aggression was significantly lower in a large aquarium with a complex habitat. Aquaria of sizes typically used in the companion animal (pet) hobby did not provide optimal welfare for cichlids housed with aggressive conspecifics. The public should be aware that this and similar species require larger aquaria with complex habitat, which elicit more natural behavior.     

Growth of the teleost eye: novel solutions to complex constraints

Synopsis The cichlid fish, Haplochromis burtoni, is highly dependent on vision for survival in its natural habitat. As is true of most teleost fishes, the eyes continue to grow throughout life without any obvious changes in visual capability. In H. burtoni, for example, retinal area may increase by 27 × in just 6 months. During growth, there is no obvious change in the visual sensitivity, visual acuity or lens quality which must all be appropriate for the enlarging eye. This requires that during growth competing constraints be met. For example, to maintain visual acuity, the number of ganglion cells per visual angle subtended on the retina must remain the same as must the convergence ratio of the cones onto those ganglion cells. In contrast, to maintain visual sensitivity, the number of rod photoreceptors per unit retinal area must remain the same. These requirements are in conflict since a larger eye may preserve acuity with fewer cells per unit area in a larger retina. In addition, the lens properties must remain the same as the animal increases in size so that the image available is of similar quality throughout life. Experiments have been performed to reveal the adaptations during growth which allow the fish to preserve its image of the world throughout life.     

Species-specific patterns of nonapeptide brain gene expression relative to pair-bonding behavior in grouping and non-grouping cichlids

Comparative studies have revealed that vasopressin–oxytocin pathways are associated with both pair bonding and grouping behavior. However, the relationship between pair bonding and grouping behavior remains unclear. In this study, our aim was to identify whether two species that differ in grouping behavior display a corresponding difference in their pair bonds, and in the underlying vasopressin–oxytocin hormonal pathways. Using two species of cichlid fishes, the highly social Neolamprologus pulcher and the non-social Telmatochromis temporalis, we measured proximity of pairs during pair bond formation, and then measured social behaviors (proximity, aggression, submission, affiliation) and brain gene expression of isotocin and arginine vasotocin (the teleost homologues of oxytocin and vasopressin, respectively), as well as their receptors, after a temporary separation and subsequent reunion of the bonded pairs. Pairs of the social species spent more time in close proximity relative to the non-social species. Rates of aggression increased in both species following the separation and reunion treatment, relative to controls that were not separated. Overall, whole brain expression of isotocin was higher in the social species relative to the non-social species, and correlated with proximity, submission, and affiliation, but only in the social species. Our results suggest that both a social and a non-social cichlid species have similar behavioral responses to a temporary separation from a mate, and we found no difference in the brain gene expression of measured hormones and receptors based on our separation–reunion treatment. However, our results highlight the importance of isotocin in mediating submissive and affiliative behaviors in cichlid fishes, and demonstrate that isotocin has species-specific correlations with socially relevant behaviors.     

Sociality, ecology, and relative brain size in lemurs

The social brain hypothesis proposes that haplorhine primates have evolved relatively large brains for their body size primarily as an adaptation for living in complex social groups. Studies that support this hypothesis have shown a strong relationship between relative brain size and group size in these taxa. Recent reports suggest that this pattern is unique to haplorhine primates; many nonprimate taxa do not show a relationship between group size and relative brain size. Rather, pairbonded social monogamy appears to be a better predictor of a large relative brain size in many nonprimate taxa. It has been suggested that haplorhine primates may have expanded the pairbonded relationship beyond simple dyads towards the evolution of complex social groups. We examined the relationship between group size, pairbonding, and relative brain size in a sample of 19 lemurs; strepsirrhine primates that last share a common ancestor with monkeys and apes approximately 75 Ma. First, we evaluated the social brain hypothesis, which predicts that species with larger social groups will have relatively larger brains. Secondly, we tested the pairbonded hypothesis, which predicts that species with a pairbonded social organization will have relatively larger brains than non-pairbonded species. We found no relationship between group size or pairbonding and relative brain size in lemurs. We conducted two further analyses to test for possible relationships between two nonsocial variables, activity pattern and diet, and relative brain size. Both diet and activity pattern are significantly associated with relative brain size in our sample. Specifically, frugivorous species have relatively larger brains than folivorous species, and cathemeral species have relatively larger brains than diurnal, but not nocturnal species. These findings highlight meaningful differences between Malagasy strepsirrhines and haplorhines, and between Malagasy strepsirrhines and nonprimate taxa, regarding the social and ecological factors associated with increases in relative brain size. The results suggest that factors such as foraging complexity and flexibility of activity patterns may have driven selection for increases in brain size in lemurs.     

Brain gangliosides and cold-adaptation in high-antarctic fish

The concentration and composition of gangliosides from the brain of eight species of Antarctic Notothenioid fishes belonging to the class of perciformes and two species of boreal fishes (tropic cichlid fish Oreochromis mossambicus; Codfish Gadus morhua) were investigated. The concentration of whole brain gangliosides in Notothenioid fishes (between 1622 and 2183 μg NeuAc/g dry wt.) was slightly lower than that in the brains of fish species, which live in warm, temperate habitats (2483 μg NeuAc/g dry wt.). The composition of brain gangliosides was completely different from that of warm adapted fish species (e.g. the tropic cichlid fish Oreochromis mossambicus). The relative concentration of polysialogangliosides (GT1b-GH) is strongly increased in all the investigated Antarctic species. They were found to have the most complex and most polar brain ganglioside pattern (high degree of sialylation and alkali-lability) within the teleosts. This may be one of the mechanisms, beside antifreeze proteins, to keep the neuronal membranes functional even below the freezing point.     

Community Structure of Fishes and Habitat Complexity on a Tropical Rocky Shore

The relationship between the variables of reef fish community structure (fish richness, fish diversity and total number of fishes) and those of habitat complexity (total surface area, substratum diversity, topographic complexity, number of holes, percent cover of turf algae, zoanthids, millepores, massive corals, bare rock, encrusting calcareous algae, urchins, other sessile organisms and Sargassum) were examined on three different rocky shores (FA, FB and FT) at Arraial do Cabo, a tropical region located on Brazilian southeastern coast (23° S, 42° W). Fish abundance and vertical distribution were assessed by a visual census technique using strip transects. Percentage cover of benthic organisms and other substratum types were calculated by replicated transects using a chain laid down on the substratum. Topographic complexity was determined by the chain link method and number of holes were estimated by direct counts on replicated transects. More than 91 fishes belonging to 37 families were seen in all study sites during one year of visual census effort. FA and FB sites had similar fish community structure and habitat complexity characteristics, while FT showed different habitat characteristics and higher fish diversity and richness, plus total number of fishes. Vertical distribution of fishes along the rocky shores studied seemed to be predictable and was determined by factors such as feeding habits and behavior, availability of refuges and social interactions. The habitat variables that best explained the higher diversity and number of fishes observed in FT site were total surface area of rocky shores and the abundance of benthic sessile invertebrates; these conditions were typical of rocky shores more exposed to wave surge.     

Gonadotropin-releasing hormone signaling in behavioral plasticity

Sex and reproduction sculpt brain and behavior throughout life and evolution. In vertebrates, gonadotropin-releasing hormone (GnRH) is essential to these processes. Recent advances have uncovered novel regulatory mechanisms in GnRH signaling, such as the initiation of sexual maturation by kisspeptins. Yet despite our increasing molecular knowledge, we know very little about environmental influences on GnRH signaling and reproductive behavior. Alternative model systems have been crucial for understanding the plasticity of GnRH effects within an organismal context. For instance, GnRH signaling is under the control of seasonal cues in songbirds, whereas social signals regulate GnRH in cichlid fishes, with crucial consequences for reproduction and behavior. Analyzing cellular signaling cascades within an organismic context is essential for an integrative understanding of GnRH function.     

Visual specialization and brain evolution in primates.

Several theories have been proposed to explain the evolution of species differences in brain size, but no consensus has emerged. One unresolved question is whether brain size differences are a result of neural specializations or of biological constraints affecting the whole brain. Here I show that, among primates, brain size variation is associated with visual specialization. Primates with large brains for their body size have relatively expanded visual brain areas, including the primary visual cortex and lateral geniculate nucleus. Within the visual system, it is, in particular, one functionally specialized pathway upon which selection has acted: evolutionary changes in the number of neurons in parvocellular, but not magnocellular, layers of the lateral geniculate nucleus are correlated with changes in both brain size and ecological variables (diet and social group size). Given the known functions of the parvocellular pathway, these results suggest that the relatively large brains of frugivorous species are products of selection on the ability to perceive and select fruits using specific visual cues such as colour. The separate correlation between group size and visual brain evolution, on the other hand, may indicate the visual basis of social information processing in the primate brain.     

Early behaviour in fishes

Synopsis The ethological approach to the study of early life histories of fishes is illustrated by examples of behavioural ontogeny in cichlid and salmonid fishes. In both species recognition and social organization, early experience is of crucial importance.Paper presented in the symposium \lsEmbryonic and larval periods of fishes: present status and significance\rs, Canadian Conference for Fisheries Research (CCFFR), Fredericton, New Brunswick, January 1977     

Is there convergence in the molecular pathways underlying the repeated evolution of sociality in African cichlids?

Despite wide variation in the complexity of social interactions across taxa, the basic behavioral components of sociality appear to be modulated by conserved hormone pathways. Specifically, the nonapeptide hormones oxytocin and vasopressin and their receptors have been implicated in regulating diverse social behaviors across vertebrates. Here, we took advantage of the repeated evolution of cooperative breeding in African cichlids to investigate whether there are consistent brain gene expression patterns of isotocin and arginine vasotocin (teleost homologues of oxytocin and vasopressin), as well as their receptors, between four closely related pairs of social (cooperative) and non-social (non-cooperative) species. We first found that the coding sequences for the five genes studied were highly conserved across the eight species. This is the first study to examine the expression of both isotocin receptors, and so we performed a phylogenetic analysis that suggests that these two isotocin receptors are paralogues that arose during the teleost genome duplication. When we then examined brain gene expression patterns relative to social system, we found that there were whole-brain gene expression differences between the social and non-social species in many of the species pairs. However, these relationships varied in both the direction and magnitude among the four species pairs. In conclusion, our results suggest high sequence conservation and species-specific gene expression patterns relative to social behavior for these candidate hormone pathways in the cichlid fishes.     

Ecology and mating competition influence sexual dimorphism in Tanganyikan cichlids

Sexual selection contributes strongly to the evolution of sexual dimorphism among animal taxa. However, recent comparative analyses have shown that evolution of sexual dimorphism can be influenced by extrinsic factors like mating system and environment, and also that different types of sexual dimorphism may present distinct evolutionary pathways. Investigating the co-variation among different types of sexual dimorphism and their association with environmental factors can therefore provide important information about the mechanisms generating variation in sexual dimorphism among contemporary species. Using phylogenetic comparative analyses comparing 49 species of Tanganyikan cichlid fishes, we first investigated the pairwise relationship between three types of sexual dimorphism [size dimorphism (SSD), colour dimorphism (COD) and shape dimorphism (SHD)] and how they were related to the strength of pre- and post-copulatory sexual selection. We then investigated the influence of ecological features on sexual dimorphism. Our results showed that although SSD was associated with the overall strength of sexual selection it was not related to other types of sexual dimorphism. Also, SSD co-varied with female size and spawning habitat, suggesting a role for female adaptations to spawn in small crevices and shells influencing SSD in this group. Further, COD and SHD were positively associated and both show positive relationships with the strength of sexual selection. Finally, the level of COD and SHD was related to habitat complexity. Our results thus highlight distinct evolutionary pathways for different types of sexual dimorphism and further that ecological factors have influenced the evolution of sexual dimorphism in Tanganyikan cichlid fishes.     

Habitat use and its implications to functional morphology: niche partitioning and the evolution of locomotory morphology in Lake Tanganyikan cichlids (Perciformes: Cichlidae)

Animal locomotory morphology, i.e. morphological features involved in locomotion, is under the influence of a diverse set of ecological and behavioral factors. In teleost fish, habitat choice and foraging strategy are major determinants of locomotory morphology. In this study, we assess the influence of habitat use and foraging strategy on important locomotory traits, namely the size of the pectoral and caudal fins and the weight of the pectoral fin muscles, as applied to one of the most astonishing cases of adaptive radiation: the species flock of cichlid fishes in East African Lake Tanganyika. We also examine the course of niche partitioning along two main habitat axes, the benthic vs. limnetic and the sandy vs. rocky substrate axis. The results are then compared with available data on the cichlid adaptive radiation of neighbouring Lake Malawi. We find that pectoral fin size and muscle weight correlate with habitat use within the water column, as well as with substrate composition and foraging strategies. Niche partitioning along the benthic–limnetic axis in Lake Tanganyikan cichlids seems to follow a similar course as in Lake Malawi, while the course of habitat use with respect to substrate composition appears to differ between the cichlid assemblages of these two lakes.     

Larger brain size indirectly increases vulnerability to extinction in mammals

Although previous studies have addressed the question of why large brains evolved, we have limited understanding of potential beneficial or detrimental effects of enlarged brain size in the face of current threats. Using novel phylogenetic path analysis, we evaluated how brain size directly and indirectly, via its effects on life history and ecology, influences vulnerability to extinction across 474 mammalian species. We found that larger brains, controlling for body size, indirectly increase vulnerability to extinction by extending the gestation period, increasing weaning age, and limiting litter sizes. However, we found no evidence of direct, beneficial, or detrimental effects of brain size on vulnerability to extinction, even when we explicitly considered the different types of threats that lead to vulnerability. Order‐specific analyses revealed qualitatively similar patterns for Carnivora and Artiodactyla. Interestingly, for Primates, we found that larger brain size was directly (and indirectly) associated with increased vulnerability to extinction. Our results indicate that under current conditions, the constraints on life history imposed by large brains outweigh the potential benefits, undermining the resilience of the studied mammals. Contrary to the selective forces that have favored increased brain size throughout evolutionary history, at present, larger brains have become a burden for mammals.     

Retention of Habitat Complexity Minimizes Disassembly of Reef Fish Communities following Disturbance: A Large-Scale Natural Experiment

High biodiversity ecosystems are commonly associated with complex habitats. Coral reefs are highly diverse ecosystems, but are under increasing pressure from numerous stressors, many of which reduce live coral cover and habitat complexity with concomitant effects on other organisms such as reef fishes. While previous studies have highlighted the importance of habitat complexity in structuring reef fish communities, they employed gradient or meta-analyses which lacked a controlled experimental design over broad spatial scales to explicitly separate the influence of live coral cover from overall habitat complexity. Here a natural experiment using a long term (20 year), spatially extensive (∼115,000 kms²) dataset from the Great Barrier Reef revealed the fundamental importance of overall habitat complexity for reef fishes. Reductions of both live coral cover and habitat complexity had substantial impacts on fish communities compared to relatively minor impacts after major reductions in coral cover but not habitat complexity. Where habitat complexity was substantially reduced, species abundances broadly declined and a far greater number of fish species were locally extirpated, including economically important fishes. This resulted in decreased species richness and a loss of diversity within functional groups. Our results suggest that the retention of habitat complexity following disturbances can ameliorate the impacts of coral declines on reef fishes, so preserving their capacity to perform important functional roles essential to reef resilience. These results add to a growing body of evidence about the importance of habitat complexity for reef fishes, and represent the first large-scale examination of this question on the Great Barrier Reef.     

Gonad development in Midas cichlids and the evolution of sex change in fishes

Some fishes mature and function as one sex and later transform to the other sex in response to social interactions. Previous evidence suggested that a change in developmental timing may be involved in the evolution of adult sex change in fishes. The most recent support for this idea came from reports that sex in the Midas cichlid, Amphilophus citrinellus, was determined by social conditions experienced at the juvenile stage. Differentiation as a male was reported to be dependent on large body size relative to group-mates, and thought to be mediated through aggressive interactions. Here I demonstrate that socially controlled sex determination does not occur as was originally reported. Previously, I found that sex was not associated with body size in juveniles either in nature or in captivity. Similarly, I found no association between aggressive behavior and sex in juveniles. I later demonstrated that socially controlled sex determination does not typically occur in the Midas cichlid and closely related species and supported an alternative mechanism to explain large body size in adult males. Finally, in the current study I analyze gonad histology of fish from the same population used by the original authors and lay to rest the idea of socially controlled sex determination in this species. Recent observations of socially controlled sex determination in juveniles of species that typically change sex at the adult stage are examples of phenotypic plasticity, not genetic variation. Therefore, juvenile socially controlled sex determination does not support a theory that a change in developmental timing is involved in the evolution of adult sex change in fishes.