RESUMO
BACKGROUND: Despite a longstanding interest in understanding how animals adapt to environments with limited nutrients, we have incomplete knowledge of the genetic basis of metabolic evolution. The Mexican tetra, Astyanax mexicanus, is a species of fish that consists of two morphotypes; eyeless cavefish that have adapted to a low-nutrient cave environment, and ancestral river-dwelling surface fish with abundant access to nutrients. Cavefish have evolved altered blood sugar regulation, starvation tolerance, increased fat accumulation, and superior body condition. To investigate the genetic basis of cavefish metabolic evolution we carried out a quantitative trait loci (QTL) analysis in surface/cave F2 hybrids. We genetically mapped seven metabolism-associated traits in hybrids that were challenged with a nutrient restricted diet. RESULTS: We found that female F2 hybrids are bigger than males and have a longer hindgut, bigger liver, and heavier gonad, even after correcting for fish size. Although there is no difference between male and female blood sugar level, we found that high blood sugar is associated with weight gain in females and lower body weight and fat level in males. We identified a significant QTL associated with 24-h-fasting blood glucose level with the same effect in males and females. Differently, we identified sex-independent and sex-dependent QTL associated with fish length, body condition, liver size, hindgut length, and gonad weight. We found that some of the genes within the metabolism QTL display evidence of non-neutral evolution and are likely to be under selection. Furthermore, we report predicted nonsynonymous changes to the cavefish coding sequence of these genes. CONCLUSIONS: Our study reveals previously unappreciated genomic regions associated with blood glucose regulation, body condition, gonad size, and internal organ morphology. In addition, we find an interaction between sex and metabolism-related traits in A. mexicanus. We reveal coding changes in genes that are likely under selection in the low-nutrient cave environment, leading to a better understanding of the genetic basis of metabolic evolution.
Assuntos
Characidae , Locos de Características Quantitativas , Animais , Evolução Biológica , Characidae/genética , Mapeamento Cromossômico , Feminino , Masculino , México , Locos de Características Quantitativas/genéticaRESUMO
Carotenoids are lipid-soluble yellow to orange pigments produced by plants, bacteria, and fungi. They are consumed by animals and metabolized to produce molecules essential for gene regulation, vision, and pigmentation. Cave animals represent an interesting opportunity to understand how carotenoid utilization evolves. Caves are devoid of light, eliminating primary production of energy through photosynthesis and, therefore, limiting carotenoid availability. Moreover, the selective pressures that favor carotenoid-based traits, like pigmentation and vision, are relaxed. Astyanax mexicanus is a species of fish with multiple river-adapted (surface) and cave-adapted populations (i.e., Tinaja, Pachón, Molino). Cavefish exhibit regressive features, such as loss of eyes and melanin pigment, and constructive traits, like increased sensory neuromasts and starvation resistance. Here, we show that, unlike surface fish, Tinaja and Pachón cavefish accumulate carotenoids in the visceral adipose tissue. Carotenoid accumulation is not observed in Molino cavefish, indicating that it is not an obligatory consequence of eye loss. We used quantitative trait loci mapping and RNA sequencing to investigate genetic changes associated with carotenoid accumulation. Our findings suggest that multiple stages of carotenoid processing may be altered in cavefish, including absorption and transport of lipids, cleavage of carotenoids into unpigmented molecules, and differential development of intestinal cell types involved in carotenoid assimilation. Our study establishes A. mexicanus as a model to study the genetic basis of natural variation in carotenoid accumulation and how it impacts physiology.
Assuntos
Carotenoides/metabolismo , Characidae/genética , Animais , Evolução Biológica , Carotenoides/análise , Cavernas , Characidae/anatomia & histologia , Characidae/metabolismo , Cromatografia Líquida de Alta Pressão , Mapeamento Cromossômico , Olho/anatomia & histologia , Feminino , Gordura Intra-Abdominal/química , Masculino , Análise de Sequência de DNA , Análise de Sequência de RNA , TranscriptomaRESUMO
Little is known about the genetic basis of behavioral choice, such as temperature preference, especially in natural populations. Thermal preference can play a key role in habitat selection, for example in aquatic species. Examining this behavior on a genetic level requires access to individuals or populations of the same species that display distinct temperature preferences. Caves provide a uniquely advantageous setting to tackle this problem, as animals colonizing caves encounter an environment that generally has a different, and far more stable, annual temperature than what is encountered on the outside. Here, we focus on cave and surface populations of Astyanax mexicanus, the Mexican tetra, and examine temperature preference and strength of temperature preference (reflected in the percent of time spent at the optimal temperature). We used a tank with a stable temperature gradient and automated tracking software to follow individual fish from each population. We found that distinct populations of A. mexicanus display differences in both temperature preference and strength of preference. Hybrid crosses established that these are multigenic traits that segregate independently from one another. Temperature preference in many aquatic animals is known to shift towards warmer temperatures following infection with parasites (akin to a fever response in humans). While surface fish infected by the ectoparasite Gyrodactylus turnbulli (a gill fluke) displayed a strong fever response, cavefish showed a significantly attenuated fever response. This work establishes A. mexicanus as a genetically tractable system in which differences in temperature preference can be studied in naturally evolved populations.