Masato Yoshizawa

Shell selection in hermit crabs is a demanding task that integrates multiple sensory cues, including visual information. Because the shell provides cryptic shelter from predation, the accuracy of visual assessment would yield higher fitness. Classically, many hermit crab species have been considered monochromatic based on the finding of only one visual pigment in surveyed species and shell preferences in a few well-studied species based on differences in shell and background brightness. However, it is unclear whether a tropical hermit crab uses the same monochromatic strategy, particularly given recent discoveries of multiple visual pigments in Decapoda species. Here, we tested shell selection in the white-banded hermit crab, Calcinus seurati: the crabs were tested for their preference between blue and green shells against either a blue or green background because most crustaceans carry visual pigments with maximum absorbances in the blue-green range (480–540 nm). The contact frequencies were then expected to be higher for shells with larger Weber contrast scores according to the reported monochromatic decisions. In contrast, the white-banded crabs exhibited a consistent preference for the green shell regardless of Weber contrast values. The result invites a reappraisal of the possibility of colour vision during shell assessment in hermit crabs.

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 cavefish ^1–3 . 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 analysis ⁴ 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.

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, a tradeoff that often occurs through expansion and contraction of chemosensory receptor gene families. The Mexican tetra (Astyanax mexicanus), with both sighted surface-dwelling and blind cave-dwelling populations, presents an ideal model for testing this tradeoff. In this study, although cavefish can sense odorants at 100 times lower concentrations than surface fish, they do not have an expanded repertoire of chemosensory receptors, increased number of olfactory sensory neurons, or enhanced expression of receptors. Instead, cavefish increased motile cilia cells on the olfactory epithelium and decreased flow rate through the olfactory pits. Pharmacological attenuation of flow rate in surface fish increased visits to the odorant source, suggesting that reduced flow rate in cavefish facilitates locating food.

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.

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.

Background: 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. Results: 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 1 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 exogenous ketone bodies, revealing that ketone bodies are pivotal molecules positively associated with social affinity. Conclusions: 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.

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.

Background: 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. Results: 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. Conclusion: Based on these findings, we propose a model explaining how the observed sensory laterality and behavioral shift could help adaptation in terms of the tradeoff in energy gain and loss during foraging according to differences in food availability among caves.