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Yoshizawa, M.

Publications and source records attributed to Yoshizawa, M..

8 recordsLinked to original sources

Evolution of novel host-microbiota coupling underlies adaptation to nutrient-scarce environments.

Animals colonizing food-limited environments need to overcome growth constraints by adapting to low, inconsistent nutritional inputs. Comparative studies of surface and cave populations of the Mexican tetra fish species Astyanax mexicanus provide a powerful system to explore evolution to food scarcity. In nutrient-scarce caves, evolved traits such as eye loss and increased fat storage have been shown to conserve energy in cavefish1-3 . However, the role of microbiota-mediated metabolism in sustaining growth and survival under food limitation remains poorly understood. Here, we demonstrate that surface and cave populations distinctly modulate their gut microbiota, with cavefish recruiting microbes whose predicted metabolites specifically promote growth under nutrient-limited conditions. Using microbiota data from three distinct dietary regimes and a fasting treatment, integrated topological data analysis4 and sparse modeling identify sugar and fatty acid degradation pathways coupled with growth in cavefish. Notably, the metabolites of these pathways are beneficial only for cavefish growth, and not for surface fish. Fasting in cavefish led to the recruitment of gut microbes capable of metabolizing aromatic compounds inaccessible to the host, whereas it recruited few microbial associates in surface fish. Our findings indicate that cavefish evolved novel host-microbiota coupling to sustain growth and resilience in their nutrient-scarce niche. We anticipate that our findings will broadly inform studies of evolution under extreme nutritional conditions and provide insights into the role of host-microbiota interactions in resilience to food scarcity at varied time scales.

evolutionary biology↗

Novel mechanisms of chemosensory adaptation to the cave environment

Smell allows animals to find food, avoid danger, and communicate through the binding of odorants to chemosensory receptors on olfactory sensory neurons. The vision-priority hypothesis predicts an antagonistic relationship between olfaction and vision, in which olfactory ability increases as visual acuity decreases along evolutionary lineages, a tradeoff that often occurs through expansion and contraction of chemosensory receptor gene families. The Mexican tetra (Astyanax mexicanus), a fish species with both sighted surface-dwelling and blind cave-dwelling populations, presents an ideal model for exploring the mechanisms underlying this tradeoff. Here we show that although cavefish can sense odorants at lower concentrations than surface fish, they do not have an expanded repertoire of chemosensory receptors, increased sensory neuron number or density, or enhanced expression of receptors compared to surface fish. Instead, cavefish have physiological adaptations to the olfactory epithelium, including more motile cilia and decreased flow rate through the olfactory pits. Pharmacological attenuation of flow rate in the olfactory pits in surface fish increased visits to the odorant source, suggesting that the reduced flow rate in cavefish is an adaptation leading to better foraging. This unexpected evolutionary path to enhanced olfaction as a compensation for loss of vision underscores the need for mechanistic understanding of comparative genomics.

evolutionary biology↗

Blind cavefish evolved food-searching behavior without changing sensory modality compared with sighted conspecies in the dark

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 similar sensory modality to surface fish in the dark, while adherence levels to stimuli were higher in cavefish. In addition, cavefish evolved an extended circling strategy to capture food, 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 ancestors of cavefish similar to surface fish may have needed little modification in food-seeking strategy to adapt to the dark.

ecology↗

Possible role of left-right asymmetry in the sensory system and behavior during adaptation to food-sparse cave environments

Laterality in relation to behavior and sensory systems is found commonly in a variety of animal taxa. Despite the advantages conferred by laterality (e.g., the startle response and complex motor activities), little is known about the evolution of laterality and its plasticity in response to ecological demands. In the present study, a comparative study model, the Mexican tetra (Astyanax mexicanus), composed of two morphotypes, i.e., riverine surface fish and cave-dwelling cavefish, was used to address the relationship between environment and laterality. The use of a machine learning-based fish posture detection system and sensory ablation revealed that the left cranial lateral line significantly supports one type of foraging behavior, i.e., vibration attraction behavior, in one cave population. Additionally, left-right asymmetric approaches toward a vibrating rod became symmetrical after fasting in one cave population but not in the other populations. Based on these findings, we propose a model explaining how the observed sensory laterality and behavioral shift could help adaptations in terms of the tradeoff in energy gain and loss during foraging according to differences in food availability among caves.

ecology↗

Metabolic shift toward ketosis in asocial cavefish increases social-like collective behavior.

Social affinity and collective behavior are nearly ubiquitous in the animal kingdom, but many lineages feature evolutionarily asocial species. These solitary species may have evolved to conserve energy in food-sparse environments. However, the mechanism by which metabolic shifts regulate social affinity is not well investigated. In this study, we used the Mexican tetra (Astyanax mexicanus), which features riverine sighted surface (surface fish) and cave-dwelling populations (cavefish), to address the impact of metabolic shifts on asociality and other cave-associated behaviors in cavefish, including repetitive turning, sleeplessness, swimming longer distances, and enhanced foraging behavior. After one month of ketosis-inducing ketogenic diet feeding, asocial cavefish exhibited significantly higher social affinity, whereas social affinity regressed in cavefish fed the standard diet. The ketogenic diet also reduced repetitive turning and swimming in cavefish. No major behavioral shifts were found regarding sleeplessness and foraging behavior, suggesting that other evolved behaviors are not largely regulated by ketosis. We further examined the effects of the ketogenic diet via supplementation with extragenic ketone bodies, revealing that ketone bodies are pivotal molecules positively associated with social affinity. Our study indicated that fish that evolved to be asocial remain capable of exhibiting social affinity under ketosis, possibly linking the seasonal food availability and sociality.

physiology↗

Social-like responses are inducible in the asocial and blind Mexican cavefish despite the continued exhibition of strong repetitive behavior

Social behaviour is a hallmark of complex animal systems; however, some species appear to have secondarily lost this social ability. In these non-social species, whether social abilities are permanently lost or suppressed is unclear. The blind cavefish Astyanax mexicanus is known to be asocial. Here, we reveal that cavefish exhibited social-like interactions in familiar environments but suppressed these interactions in stress-associated unfamiliar environments. Furthermore, the level of suppression in sociality was positively correlated with that of stereotypic repetitive behaviour, as seen in mammals. Treatment with a human antipsychotic drug targeting the dopaminergic system induced social-like interactions in cavefish, even in unfamiliar environments, while reducing repetitive behaviour. Overall, these results suggest that the antagonistic relationship between repetitive and social-like behaviours is deeply shared from teleosts through mammals.

evolutionary biology↗

Dual Roles of the Retinal Pigment Epithelium and Lens in Cavefish Eye Degeneration

Astyanax mexicanus consists of two forms, a sighted surface dwelling form (surface fish) and a blind cave-dwelling form (cavefish). Embryonic eyes are initially formed in cavefish but they are subsequently arrested in growth and degenerate during larval development. Previous lens transplantation studies have shown that the lens plays a central role in cavefish eye loss. However, several lines of evidence suggest that additional factors, such as the retinal pigment epithelium (RPE), which is morphologically altered in cavefish, could also be involved in the eye regression process. To explore the role of the RPE in cavefish eye degeneration, we generated an albino eyed (AE) strain by artificial selection for hybrid individuals with large eyes and a depigmented RPE. The AE strain exhibited an RPE lacking pigment granules and showed reduced expression of the RPE specific enzyme retinol isomerase, allowing eye development to be studied by lens ablation in an RPE background resembling cavefish. We found that lens ablation in the AE strain had stronger negative effects on eye growth than in surface fish, suggesting that an intact RPE is required for normal eye development. We also found that the AE strain develops a cartilaginous sclera lacking boney ossicles, a trait similar to cavefish. Extrapolation of the results to cavefish suggests that the RPE and lens have dual roles in eye degeneration, and that deficiencies in the RPE may be associated with evolutionary changes in scleral ossification.

developmental biology↗

The role of gene flow in rapid and repeated evolution of cave related traits in Mexican tetra, Astyanax mexicanus

Understanding the molecular basis of repeated evolved phenotypes can yield key insights into the evolutionary process. Quantifying the amount of gene flow between populations is especially important in interpreting mechanisms of repeated phenotypic evolution, and genomic analyses have revealed that admixture is more common between diverging lineages than previously thought. In this study, we resequenced and analyzed nearly 50 whole genomes of the Mexican tetra from three blind cave populations, two surface populations, and outgroup samples. We confirmed that cave populations are polyphyletic and two Astyanax mexicanus lineages are present in our dataset. The two lineages likely diverged [~]257k generations ago, which, assuming 1 generation per year, is substantially younger than previous mitochondrial estimates of 5-7mya. Divergence of cave populations from their phylogenetically closest surface population likely occurred between [~]161k - 191k generations ago. The favored demographic model for most population pairs accounts for divergence with secondary contact and heterogeneous gene flow across the genome, and we rigorously identified abundant gene flow between cave and surface fish, between caves, and between separate lineages of cave and surface fish. Therefore, the evolution of cave-related traits occurred more rapidly than previously thought, and trogolomorphic traits are maintained despite substantial gene flow with surface populations. After incorporating these new demographic estimates, our models support that selection may drive the evolution of cave-derived traits, as opposed to the classic hypothesis of disuse and drift. Finally, we show that a key QTL is enriched for genomic regions with very low divergence between caves, suggesting that regions important for cave phenotypes may be transferred between caves via gene flow. In sum, our study shows that shared evolutionary history via gene flow must be considered in studies of independent, repeated trait evolution.

evolutionary biology↗