Sequential developmental events, starting from the moment of fertilization, are crucial for the acquisition of animal body plan. Subtle modifications in such early events are likely to have major ...impacts in later morphogenesis, bringing along morphological diversification. Here, comparing the blind cave and the surface morphotypes of
fish, we found heterochronies during gastrulation that produce organizer and axial mesoderm tissues with different properties (including differences in the expression of
) that may have contributed to cavefish brain evolution. These variations observed during gastrulation depend fully on maternal factors. The developmental evolution of retinal morphogenesis and hypothalamic patterning are among those traits that retained significant maternal influence at larval stages. Transcriptomic analysis of fertilized eggs from both morphotypes and reciprocal F
hybrids showed a strong and specific maternal signature. Our work strongly suggests that maternal effect genes and developmental heterochronies that occur during gastrulation have impacted morphological brain change during cavefish evolution.
Acoustic communication allows the exchange of information within specific contexts and during specific behaviors. The blind, cave-adapted and the sighted, river-dwelling morphs of the species ...Astyanax mexicanus have evolved in markedly different environments. During their evolution in darkness, cavefish underwent a series of morphological, physiological and behavioral changes, allowing the study of adaptation to drastic environmental change. Here we discover that Astyanax is a sonic species, in the laboratory and in the wild, with sound production depending on the social contexts and the type of morph. We characterize one sound, the "Sharp Click", as a visually-triggered sound produced by dominant surface fish during agonistic behaviors and as a chemosensory-, food odor-triggered sound produced by cavefish during foraging. Sharp Clicks also elicit different reactions in the two morphs in play-back experiments. Our results demonstrate that acoustic communication does exist and has evolved in cavefish, accompanying the evolution of its behaviors.
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.
Within the species Astyanax mexicanus, there are several interfertile populations of river-dwelling sighted fish and cave-dwelling blind fish which have evolved morphological and behavioral ...adaptations, the origins of which are unknown. Here, we have investigated the neural, genetic, and developmental bases for the evolution of aggressive behavior in this teleost.
We used an intruder-resident behavioral assay to compare aggressiveness quantitatively (attack counts) and qualitatively (pattern and nature of attacks) between the surface and cave populations of Astyanax. Using this paradigm, we characterize aggressive behavior in surface fish, bring support for the genetic component of this trait, and show that it is controlled by raphe serotonergic neurons and that it corresponds to the establishment of dominance between fish. Cavefish have completely lost such aggressive/dominance behavior. The few attacks performed by cavefish during the behavioral test instead correspond to food-seeking behavior, driven by the developmental evolution of their hypothalamic serotonergic paraventricular neurons, itself due to increased Sonic Hedgehog signaling during early forebrain embryogenesis.
We propose that during evolution and adaptation to their cave habitat, cavefish have undergone a behavioral shift, due to modifications of their serotonergic neuronal network. They have lost the typical aggressive behavior of surface fish and evolved a food-seeking behavior that is probably more advantageous to surviving in the dark. We have therefore demonstrated a link between the development of a neuronal network and the likely adaptive behaviors it controls.
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► Astyanax cavefish have lost aggressive behavior during adaptation to life in the dark ► Astyanax raphe serotonergic neurons control social behavior ► Astyanax hypothalamic serotonergic neurons control homeostatic functions ► The development of a neuronal network links to the behaviors it controls
The surface morph of the Mexican tetra fish (Astyanax mexicanus) exhibits strong territoriality behavior and high levels of aggression. In contrast, the eyeless cave-adapted morph from Sierra de El ...Abra, México, rarely are aggressive and have totally lost the territorial behavior. These behaviors are part of what has been called the cavefish behavioral syndrome. Here, we report that several Astyanax cave populations of Sierra de Guatemala, unlike those reported for the Sierra de El Abra cave populations, display significant territoriality and aggression when confined into a reduced space. We discuss divergent evolutionary trajectories in terms of agonistic behavior for cavefish populations inhabiting different mountain ranges.
Animals are adapted to their natural habitats and lifestyles. Their brains perceive the external world via their sensory systems, compute information together with that of internal states and ...autonomous activity, and generate appropriate behavioral outputs. However, how do these processes evolve across evolution? Here, focusing on the sense of olfaction, we have studied the evolution in olfactory sensitivity, preferences, and behavioral responses to six different food-related amino acid odors in the two eco-morphs of the fish Astyanax mexicanus. To this end, we have developed a high-throughput behavioral setup and pipeline of quantitative and qualitative behavior analysis, and we have tested 489 six-week-old Astyanax larvae. The blind, dark-adapted morphs of the species showed markedly distinct basal swimming patterns and behavioral responses to odors, higher olfactory sensitivity, and a strong preference for alanine, as compared to their river-dwelling eyed conspecifics. In addition, we discovered that fish have an individual 'swimming personality', and that this personality influences their capability to respond efficiently to odors and find the source. Importantly, the personality traits that favored significant responses to odors were different in surface fish and cavefish. Moreover, the responses displayed by second-generation cave x surface F2 hybrids suggested that olfactory-driven behavior and olfactory sensitivity is a quantitative genetic trait. Our findings show that olfactory processing has rapidly evolved in cavefish at several levels: detection threshold, odor preference, and foraging behavior strategy. Cavefish is therefore an outstanding model to understand the genetic, molecular, and neurophysiological basis of sensory specialization in response to environmental change.
Cavefish populations belonging to the Mexican tetra species Astyanax mexicanus are outstanding models to study the tempo and mode of adaptation to a radical environmental change. They are currently ...assigned to two main groups, the so-called "old" and "new" lineages, which would have populated several caves independently and at different times. However, we do not have yet accurate estimations of the time frames of evolution of these populations.
We reanalyzed the geographic distribution of mitochondrial and nuclear DNA polymorphisms and we found that these data do not support the existence of two cavefish lineages. Using IMa2, a program that allows dating population divergence in addition to demographic parameters, we found that microsatellite polymorphism strongly supports a very recent origin of cave populations (< 20,000 years). We identified a large number of single-nucleotide polymorphisms (SNPs) in transcript sequences of pools of embryos (Pool-seq) belonging to Pachón cave population and a surface population from Texas. Based on summary statistics that can be computed with this SNP data set together with simulations of evolution of SNP polymorphisms in two recently isolated populations, we looked for sets of demographic parameters that allow the computation of summary statistics with simulated populations that are similar to the ones with the sampled populations. In most simulations for which we could find a good fit between the summary statistics of observed and simulated data, the best fit occurred when the divergence between simulated populations was less than 30,000 years.
Although it is often assumed that some cave populations have a very ancient origin, a recent origin of these populations is strongly supported by our analyses of independent sets of nuclear DNA polymorphism. Moreover, the observation of two divergent haplogroups of mitochondrial and nuclear genes with different geographic distributions support a recent admixture of two divergent surface populations, before the isolation of cave populations. If cave populations are indeed only several thousand years old, many phenotypic changes observed in cavefish would thus have mainly involved the fixation of genetic variants present in surface fish populations and within a very short period of time.
Abstract
Evolution sometimes proceeds by loss, especially when structures and genes become dispensable after an environmental shift relaxes functional constraints. Subterranean vertebrates are ...outstanding models to analyze this process, and gene decay can serve as a readout. We sought to understand some general principles on the extent and tempo of the decay of genes involved in vision, circadian clock, and pigmentation in cavefishes. The analysis of the genomes of two Cuban species belonging to the genus Lucifuga provided evidence for the largest loss of eye-specific genes and nonvisual opsin genes reported so far in cavefishes. Comparisons with a recently evolved cave population of Astyanax mexicanus and three species belonging to the Chinese tetraploid genus Sinocyclocheilus revealed the combined effects of the level of eye regression, time, and genome ploidy on eye-specific gene pseudogenization. The limited extent of gene decay in all these cavefishes and the very small number of loss-of-function mutations per pseudogene suggest that their eye degeneration may not be very ancient, ranging from early to late Pleistocene. This is in sharp contrast with the identification of several vision genes carrying many loss-of-function mutations in ancient fossorial mammals, further suggesting that blind fishes cannot thrive more than a few million years in cave ecosystems.
The vertebrate retinas originate from a specific anlage in the anterior neural plate called the eye field. Its identity is conferred by a set of 'eye transcription factors', whose combinatorial ...expression has been overlooked. Here, we use the dimorphic teleost Astyanax mexicanus, which develops proper eyes in the wild type and smaller colobomatous eyes in the blind cavefish embryos, to unravel the molecular anatomy of the eye field and its variations within a species. Using a series of markers (rx3, pax6a, cxcr4b, zic1, lhx2, emx3 and nkx2.1a), we draw a comparative 3D expression map at the end of gastrulation/onset of neurulation, which highlights hyper-regionalization of the eye field into sub-territories of distinct sizes, shapes, cell identities and combinatorial gene expression levels along the three body axes. All these features show significant variations in the cavefish natural mutant. We also discover sub-domains within the prospective telencephalon and characterize cell identities at the frontiers of the eye field. We propose putative fates for some of the characterized eye-field subdivisions, and suggest the existence of a trade-off between some subdivisions in the two Astyanax morphs on a micro-evolutionary scale.
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