An Asymmetric Genetic Signal Associated with Mechanosensory Expansion in Cave-Adapted Fish
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S S symmetry Communication An Asymmetric Genetic Signal Associated with Mechanosensory Expansion in Cave-Adapted Fish 1, , 2 2, , Amanda K. Powers * y, Tyler E. Boggs and Joshua B. Gross * y 1 Department of Genetics, Blavatnik Institute at Harvard Medical School, Boston, MA 02138, USA 2 Department of Biological Sciences, University of Cincinnati, Cincinnati, OH 45227, USA; [email protected] * Correspondence: [email protected] (A.K.P.); [email protected] (J.B.G.); Tel.: +1-617-432-7618 (A.K.P.); +1-513-556-9708 (J.B.G.) Authors contributed equally. y Received: 7 October 2020; Accepted: 24 November 2020; Published: 26 November 2020 Abstract: A key challenge in contemporary biology is connecting genotypic variation to phenotypic diversity. Quantitative genetics provides a powerful technique for identifying regions of the genome that covary with phenotypic variation. Here, we present a quantitative trait loci (QTL) analysis of a natural freshwater fish system, Astyanax mexicanus, that harbors two morphs corresponding to a cave and surface fish. Following their divergence ~500 Kya, cavefish have adapted to the extreme pressures of the subterranean biome. As a consequence, cavefish have lost numerous features, but evolved gains for a variety of constructive features including behavior. Prior work found that sensory tissues (neuromasts) present in the “eye orbit” region of the skull associate with sensitivity to vibrations in water. This augmented sensation is believed to facilitate foraging behavior in the complete darkness of a cave, and may impact on evolved lateral swimming preference. To this point, however, it has remained unclear how morphological variation integrates with behavioral variation through heritable factors. Using a QTL approach, we discovered the genetic architecture of neuromasts present in the eye orbit region, demonstrating that this feature is under genetic control. Interestingly, linked loci were asymmetric–signals were detected using only data collected from the right, but not left, side of the face. This finding may explain enhanced sensitivity and/or feedback of water movements mediating a lateral swimming preference. The locus we discovered based on neuromast position maps near established QTL for eye size and a facial bone morphology, raising the intriguing possibility that eye loss, sensory expansion, and the cranial skeleton may be integrated for evolving adaptive behaviors. Thus, this work will further our understanding of the functional consequence of key loci that influence the evolutionary origin of changes impacting morphology, behavior, and adaptation. Keywords: craniofacial; intramembranous; neuromast; lateral line; QTL analysis 1. Introduction The blind Mexican tetra is an emerging model system for examining the genetic and cellular basis for cranial asymmetry [1–3]. This freshwater fish species, Astyanax mexicanus, includes two morphotypes inhabiting distinct biomes. Cave morphs are restricted to the complete darkness of limestone caves in the Sierra de El Abra region of Northeastern Mexico. As a consequence of life in complete darkness for several hundred thousand years, cave morphs have lost their eyes and pigmentation, but gained several features enabling adaption to this extreme environment [4,5]. Closely-related surface morphs are found broadly distributed throughout the watershed surrounding these caves and, in contrast to cave morphs, demonstrate features typical of teleost fish with normal Symmetry 2020, 12, 1951; doi:10.3390/sym12121951 www.mdpi.com/journal/symmetry Symmetry 2020, 12, 1951 2 of 10 visionSymmetry and 20 pigmentation.20, 12, x FOR PEER REVIEW Surface morphs also have largely symmetric characteristics across2 of 11 the left-rightwith normal axis with vision little and variation pigmentation. [6]. In contrast,Surface morphs cave-dwelling also have morphs largely have symmetric evolved characteristics extreme cranial asymmetries.across the left This-right asymmetry axis with little is manifested variation [6] in,. In at contrast, least, three cave principal-dwelling features.morphs have First, evolved cavefish demonstrateextreme cranial a “bend” asymmetries. in their This skulls asymmetry along the is antero-posterior manifested in, at least, axis that three is principal most often features. biased First, to the leftcavefish [7]. Second, demonstrate the dermal a “bend bones” in thattheir encircleskulls along the eyethe antero orbit are-posterior frequently axis that fused is most (synostosed) often biased in an irregularto the left pattern [7]. Second, across thethe left-rightdermal bones axis [that6,8, 9encircle]. Finally, the the eye largest orbit are bone frequently of the circumorbital fused (synostosed) complex, thein third an irregular suborbital pattern (SO3, across synonymous the left- withright infraorbital)axis [6,8,9]. Finally, bone, is the commonly largest bone fragmented of the circumorbital in an irregular architecturecomplex, the across third the suborbital lateral cranial (SO3, synonymous complex [8– with11]. infraorbital) bone, is commonly fragmented in anDespite irregular our architecture knowledge across of the the developmental lateral cranial origin complex of asymmetric [8–11]. features in cavefish, an adaptive explanationDespite for our these knowledge asymmetries of the remainsdevelopmental largely origin unknown. of asymmetric Specifically, features it in is cavefish, unclear an how morphologicaladaptive explanation asymmetry for these may asymmetries influence behavioral remains largely differences unknown. in the Specifically, blind cave it morphs. is unclear One how clue maymorphological be a form of directionalasymmetry biasmay in influence swimming behavioral patterns. differences Prior research in the demonstrated blind cave morphs. that cave-adapted One clue morphsmay be swim a form in a counterclockwiseof directional bias orientation in swimming when patterns. sampling Prior novel research objects. demonstrated However, this that swimming cave- patternadapted diminishes morphs swim once thein a object counterclockwise is no longer novelorientation [12]. Zebrafishwhen sampling use right-sided novel objects vision. However, preferentially this forswimming novel objects pattern [13]. diminishes Social stimuli once are the preferentially object is no longer viewed novel with [12] left-sided. Zebrafish vision use right [14].-sided This suggestsvision thatpreferentially asymmetric for behavioral novel objects phenotypes [13]. Social evolving stimuli in are cavefish preferentially may represent viewed wi a transferth left-sided of the vision lateral [14]. This suggests that asymmetric behavioral phenotypes evolving in cavefish may represent a sensory regulation of vision demonstrated in sighted teleosts [12]. transfer of the lateral sensory regulation of vision demonstrated in sighted teleosts [12]. Touch sensitivity in cavefish is mediated by the lateral line, which is a sensory system comprised Touch sensitivity in cavefish is mediated by the lateral line, which is a sensory system comprised of mechanosensory neuromasts (Figure1A–C) providing positional information in response to water of mechanosensory neuromasts (Figure 1A–C) providing positional information in response to water movement. Yoshizawa et al. (2010) discovered that sensory neuromasts mediate the “vibration movement. Yoshizawa et al. (2010) discovered that sensory neuromasts mediate the “vibration attraction”attraction” response response in in cave cave morphs morphs [ 15[15]].. NeuromastsNeuromasts distributed distributed within within the the “eye “eye orbit” orbit” region region of ofthe the faceface (Figure (Figure1D) 1D) seem seem to to be be particularly particularly important important inin mediatingmediating the attraction attraction to to vibrating vibrating movement movement in thein the water. water. It is It unclear, is unclear, however, however, whether whether morphological morphological asymmetry asymmetry in cranial in cranial neuromasts neuromasts influence behavioralinfluence asymmetrybehavioral asymmetry in cave morphs. in caveIf morphs. a relationship If a relationship exists between exists asymmetricbetween asymmetric neuromast distributionneuromast anddistribution lateral swimmingand lateral preference,swimming preference, one may expectone may to findexpect fixed to find genetic fixed di geneticfferences betweendifferences morphotypes. between morphotypes. FigureFigure 1. 1.Cavefish Cavefish exhibit exhibit superficial superficial neuromastsneuromasts within the the empty empty eye eye orbit. orbit. Surface Surface fish fish have have large, large, roundround eyes eyes encircled encircled by by semi-ossified semi-ossified canalscanals ((A). The infraorbital canal canal runs runs through through the the suborbital suborbital bonesbones (SO3 (SO3 shown shown in red)in red) and and in surfacein surface fish fish (B), ( actsB), acts as a as boundary a bounda betweenry between the eyethe orbit,eye orbit, dermal dermal bones, andbones the, superficial and the superficial neuromasts neuromasts that reside that on thereside surface on the of thesurface bones. of the In contrast,bones. In eye contrast, regression eye in cavefishregression causes in cavefish the orbit causes to collapse the orbit by disrupting to collapse the by positioningdisrupting the of facialpositioning bones, of canals, facial andbones, neuromasts canals, (C).and Furthermore, neuromasts the(C). sizeFurthermore, of the eye the orbit size and of the position eye orbit of facialand position bones