Search

In nature, animals must navigate to forage according to their sensory inputs. Different species use different sensory modalities to locate food efficiently. For teleosts, food emits visual, mechanical, chemical, and/or possibly weak-electrical signals, which can be detected by optic, auditory/lateral line, and olfactory/taste buds sensory systems. However, how fish respond to and use different sensory inputs when locating food, as well as the evolution of these sensory modalities, remain unclear. We examined the Mexican tetra, Astyanax mexicanus, which is composed of two different morphs: a sighted riverine (surface fish) and a blind cave morph (cavefish). Compared with surface fish, cavefish have enhanced non-visual sensory systems, including the mechanosensory lateral line system, chemical sensors comprising the olfactory system and taste buds, and the auditory system to help navigate toward food sources. We tested how visual, chemical, and mechanical stimuli evoke food-seeking behavior. In contrast to our expectations, both surface fish and cavefish did not follow a gradient of chemical stimulus (food extract) but used it as a cue for the ambient existence of food. Surface fish followed visual cues (red plastic beads and food pellets), but, in the dark, were likely to rely on mechanosensors-the lateral line and/or tactile sensor-as cavefish did. Our results indicate cavefish used a similar sensory modality to surface fish in the dark, while affinity levels to stimuli were higher in cavefish. In addition, cavefish evolved an extended circling strategy to forage, which may yield a higher chance to capture food by swimming-by the food multiple times instead of once through zigzag motion. In summary, we propose that ancestors of cavefish, similar to the modern surface fish, evolved extended food-seeking behaviors, including circling motion, to adapt to the dark., Competing Interests: The authors have declared that no competing interests exist., (Copyright: © 2024 Kuball et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)

Fish display a remarkable diversity of social behaviors, both within and between species. While social behaviors are likely critical for survival, surprisingly little is known about how they evolve in response to changing environmental pressures. With its highly social surface form and multiple populations of a largely asocial, blind, cave-dwelling form, the Mexican tetra, Astyanax mexicanus, provides a powerful model to study the evolution of social behavior. Here we use motion tracking and analysis of swimming kinematics to quantify social swimming in four Astyanax mexicanus populations. In the light, surface fish school, maintaining both close proximity and alignment with each other. In the dark, surface fish no longer form coherent schools, however, they still show evidence of an attempt to align and maintain proximity when they find themselves near another fish. In contrast, cavefish from three independently-evolved populations (Pachón, Molino, Tinaja) show little preference for proximity or alignment, instead exhibiting behaviors that suggest active avoidance of each other. Two of the three cave populations we studied also slow down when more fish are present in the tank, a behavior which is not observed in surface fish in light or the dark, suggesting divergent responses to conspecifics. Using data-driven computer simulations, we show that the observed reduction in swimming speed is sufficient to alter the way fish explore their environment: it can increase time spent exploring away from the walls. Thus, the absence of schooling in cavefish is not merely a consequence of their inability to see, but may rather be a genuine behavioral adaptation that impacts the way they explore their environment., Competing Interests: The authors have declared that no competing interests exist.

Knodus nuptialis n. sp. is described from the Rio Curuá drainage, Rio Xingu basin, Brazil. It can be diagnosed from its congeners by having dentary teeth decreasing gradually in size posteriorly, outer premaxillary teeth row with five cusps, 12-15 branched anal-fin rays and a single humeral spot. The species presents notable sexual dimorphism consisting of densely concentrated nuptial tubercles on head, body, and fins, gill-gland, and bony hooks in the anal fin of mature males. It was found that these sexually dimorphic features are useful and functional in males of the new species only during the reproductive season and after this period, they become atrophied, and eventually disappear. The list of characiform species presenting breeding tubercles is updated and nine species and two genera of the Characidae, Deuterodon and Bryconacidnus, are for the first time reported to have breeding tubercles., Competing Interests: The authors have declared that no competing interests exist.

The diploid genotypes of males are widely thought to determine sperm phenotypes, yet recent work shows that the haploid genetics of the individual sperm cell also contributes significantly. We tested seven sperm phenotypes, flagellar length and six behaviors, looking for correlations between genetic and phenotypic variability. While flagellar length appears to be controlled by the diploid genotype of the source, variation in three of the behavioral phenotypes, linearity, wobble, and progression are significantly correlated with the heterozygosity of the male producer. Because males that are more genetically variable produce a sperm set that is more diverse in its haploid genotypes, we suggest that the correlations may reflect significant haploid genetic control of sperm swimming behaviors., Competing Interests: The authors have declared that no competing interests exist.

Fish reproductive patterns are very diverse in terms of breeding frequency, mating system, sexual dimorphisms and selection, mate choice, spawning site choice, courtship patterns, spawning behaviors and parental care. Here we have compared the breeding behavior of the surface-dwelling and cave-dwelling morphs of the characiform A. mexicanus, with the goals of documenting the spawning behavior in this emerging model organism, its possible evolution after cave colonization, and the sensory modalities involved. Using infrared video recordings, we showed that cave and surface Astyanax spawning behavior is identical, occurs in the dark, and can be divided into 5 rapid phases repeated many times, about once per minute, during spawning sessions which last about one hour and involve one female and several males. Such features may constitute "pre-adaptive traits" which have facilitated fish survival after cave colonization, and may also explain how the two morphs can hybridize in the wild and in the laboratory. Accordingly, cross-breeding experiments involving females of one morphotype and males of the other morphotype showed the same behavior including the same five phases. However, breeding between cavefish females and surface fish males was more frequent than the reverse. Finally, cavefish female pheromonal solution was able to trigger strong behavioral responses in cavefish males-but not on surface fish males. Lastly, egg production seemed higher in surface fish females than in cavefish females. These results are discussed with regards to the sensory modalities involved in triggering reproductive behavior in the two morphs, as well as its possible ongoing evolution., Competing Interests: The authors have declared that no competing interests exist.

Fishes use multimodal signals during both inter- and intra-sexual displays to convey information about their sex, reproductive state, and social status. These complex behavioral displays can include visual, auditory, olfactory, tactile, and hydrodynamic signals, and the relative role of each sensory channel in these complex multi-sensory interactions is a common focus of neuroethology. The mechanosensory lateral line system of fishes detects near-body water movements and is implicated in a variety of behaviors including schooling, rheotaxis, social communication, and prey detection. Cobalt chloride is commonly used to chemically ablate lateral line neuromasts, thereby eliminating water-movement cues to test for mechanosensory-mediated behavioral functions. However, cobalt acts as a nonspecific calcium channel antagonist and could potentially disrupt function of all superficially located sensory receptor cells, including those for chemosensing. Here, we examined whether CoCl2 treatment used to ablate the lateral line system also impairs olfaction in three freshwater fishes, the African cichlid fish Astatotilapia burtoni, goldfish Carassius auratus, and the Mexican blind cavefish Astyanax mexicanus. To examine the impact of CoCl2 on the activity of peripheral receptors, we quantified DASPEI fluorescence intensity of the olfactory epithelium from fish exposed to control and CoCl2 solutions. In addition, we examined brain activation in olfactory processing regions of A. burtoni immersed in either control or cobalt solutions. All three species exposed to CoCl2 had decreased DASPEI staining of the olfactory epithelium, and in A. burtoni, cobalt treatment caused reduced neural activation in olfactory processing regions of the brain. To our knowledge this is the first empirical evidence demonstrating that the same CoCl2 treatment used to ablate the lateral line system also impairs olfactory function. These data have important implications for the use of CoCl2 in future research and suggest that previous studies using CoCl2 should be reinterpreted in the context of both impaired mechanoreception and olfaction.

Astyanax mexicanus, a teleost fish that exists in a river-dwelling surface form and multiple cave-dwelling forms, is an excellent system for studying the genetic basis of evolution. Cavefish populations, which independently evolved from surface fish ancestors multiple times, have evolved a number of morphological and behavioral traits. Quantitative trait loci (QTL) analyses have been performed to identify the genetic basis of many of these traits. These studies, combined with recent sequencing of the genome, provide a unique opportunity to identify candidate genes for these cave-specific traits. However, tools to test the requirement of these genes must be established to evaluate the role of candidate genes in generating cave-specific traits. To address this need, we designed transcription activator-like effector nucleases (TALENs) to target two genes that contain coding changes in cavefish relative to surface fish and map to the same location as QTL for pigmentation, oculocutaneous albinism 2 (oca2) and melanocortin 1 receptor (mc1r). We found that surface fish genes can be mutated using this method. TALEN-induced mutations in oca2 result in mosaic loss of melanin pigmentation visible as albino patches in F0 founder fish, suggesting biallelic gene mutations in F0s and allowing us to evaluate the role of this gene in pigmentation. The pigment cells in the albino patches can produce melanin upon treatment with L-DOPA, behaving similarly to pigment cells in albino cavefish and providing additional evidence that oca2 is the gene within the QTL responsible for albinism in cavefish. This technology has the potential to introduce a powerful tool for studying the role of candidate genes responsible for the evolution of cavefish traits.

The eyed surface form and eyeless cave form of the Mexican tetra Astyanax mexicanus experience stark differences in the daily periodicities of light, food and predation, factors which are likely to have a profound influence on metabolism. We measured the metabolic rate of Pachón cave and surface fish at a fixed swimming speed under light/dark and constant dark photoperiods. In constant darkness surface forms exhibited a circadian rhythm in metabolism with an increase in oxygen demand during the subjective daytime, whereas cave forms did not. The lack of circadian rhythm in metabolism leads to a 27% energy savings for Pachón cave fish compared to surface fish when comparing both forms in their natural photoperiods. When surface forms were tested under constant dark conditions they expended 38% more energy than cave forms under equivalent conditions. Elimination of the circadian rhythm in metabolism may be a general feature of animals that live in perpetually dark food-limited environments such as caves or the deep sea.

The relationship between growth rate and environmental space is an unresolved issue in teleosts. While it is known from aquaculture studies that stocking density has a negative relationship to growth, the underlying mechanisms have not been elucidated, primarily because the growth rate of populations rather than individual fish were the subject of all previous studies. Here we investigate this problem in the teleost Astyanax mexicanus, which consists of a sighted surface-dwelling form (surface fish) and several blind cave-dwelling (cavefish) forms. Surface fish and cavefish are distinguished by living in spatially contrasting environments and therefore are excellent models to study the effects of environmental size on growth. Multiple controlled growth experiments with individual fish raised in confined or unconfined spaces showed that environmental size has a major impact on growth rate in surface fish, a trait we have termed space dependent growth (SDG). In contrast, SDG has regressed to different degrees in the Pachón and Tinaja populations of cavefish. Mating experiments between surface and Pachón cavefish show that SDG is inherited as a dominant trait and is controlled by multiple genetic factors. Despite its regression in blind cavefish, SDG is not affected when sighted surface fish are raised in darkness, indicating that vision is not required to perceive and react to environmental space. Analysis of plasma cortisol levels showed that an elevation above basal levels occurred soon after surface fish were exposed to confined space. This initial cortisol peak was absent in Pachón cavefish, suggesting that the effects of confined space on growth may be mediated partly through a stress response. We conclude that Astyanax reacts to confined spaces by exhibiting SDG, which has a genetic component and shows evolutionary regression during adaptation of cavefish to confined environments.