Sensory evolution in blind cavefish is driven by early embryonic events during gastrulation and neurulation

Abstract

Natural variations in sensory systems constitute adaptive responses to the environment. Here, we compared sensory placode development in the blind cave-adapted morph and the eyed riverdwelling morph of Astyanax mexicanus. Focusing on the lens and olfactory placodes, we found a trade-off between these two sensory components in the two morphs: from neural plate stage onwards, cavefish have larger olfactory placodes and smaller lens placodes. In a search for developmental mechanisms underlying cavefish sensory evolution, we analyzed the roles of Shh, Fgf8 and Bmp4 signaling, which are known to be fundamental in patterning the vertebrate head and are subtly modulated in space and time during cavefish embryogenesis. Modulating these signaling systems at the end of gastrulation shifted the balance toward a larger olfactory derivative. Olfactory tests to assess potential behavioral outcomes of such developmental evolution revealed that Astyanax cavefish are able to respond to a 10 5 -fold lower concentration of amino acids than their surface-dwelling counterparts. We suggest that similar evolutionary developmental mechanisms may be used throughout vertebrates to drive adaptive sensory specializations according to lifestyle and habitat.

Contrasting feeding habits of post-larval and adult Astyanax cavefish

“…Three of these observations were in adult fish (Hüppop 1987;Yoshizawa et al 2010;Wilkens and Hüppop 1986), and two supported that the enhanced skills were already in place as early as 25 days after birth (Espinasa et al 2014;Hinaux et al 2016). For example, Hüppop (1987) showed that under competitive conditions, cavefish found about 80% of all pieces of beef-heart muscle provided in the dark whereas the epigean fish were successful at finding only 20%.…”

“…Multiple morphological and behavioural attributes have been described to support this statement, such as a higher number of taste buds (Yamamoto et al 2009;Varatharasan et al 2009), higher chemosensory capabilities (Protas et al 2008;Bibliowicz et al 2013;Hinaux et al 2016), an enhanced number of cranial neuromasts (Yoshizawa et al 2012), modulation in early developmental signalling pathways influencing brain development and organization (Yamamoto et al 2004;Pottin et al 2011), and a behaviourally more efficient posture with respect to the substrate when bottom feeding (Schemmel 1980).…”

“…Direct measurements of the size of the olfactory pits have shown that eyeless cavefish have a wider olfactory pit than eyed surface fish. The width of the olfactory pit is on average 12.9% larger due to the eyedependent developmental processes (Yamamoto et al 2003;Hinaux et al 2016). An enlarged olfactory pit could result in an enhanced sense of smell, which could directly correlate with the feeding skills of eyeless fish (Bibliowicz et al 2013).…”

“…An enlarged olfactory pit could result in an enhanced sense of smell, which could directly correlate with the feeding skills of eyeless fish (Bibliowicz et al 2013). Indeed, 30 dayold juvenile cavefish were recently shown to have outstanding olfactory capabilities at a magnitude 105 higher than surface fish for food-related amino-acid odorant cues (Hinaux et al 2016).…”

Cancer Evo-Dev, a novel hypothesis derived from studies on hepatitis B virus-induced carcinogenesis

“…from single cell creatures to multicellular creatures, and from aquatic creatures and amphibian to terrestrial mammals [ Figure 3]. Furthermore, some evolutionarily conserved molecular networks such as HOX, Hedgehog, and Myc play important roles in the developmental process [66][67][68][69][70][71][72] , indicating development and evolution share some inherent mechanisms. During the past 20 years, the discovery of conserved gene networks that control embryonic development and the ability to examine genomic records has revolutionized Darwinian evolutionism that animal relationships had to be deduced by observation of external morphological characteristics.…”