Genetic basis of eye and pigment loss in the cave crustacean, Asellus aquaticus

Abstract

Understanding the process of evolution is one of the great challenges in biology. Cave animals are one group with immense potential to address the mechanisms of evolutionary change. Amazingly, similar morphological alterations, such as enhancement of sensory systems and the loss of eyes and pigmentation, have evolved multiple times in a diverse assemblage of cave animals. Our goal is to develop an invertebrate model to study cave evolution so that, in combination with a previously established vertebrate cave system, we can address genetic questions concerning evolutionary parallelism and convergence. We chose the isopod crustacean, Asellus aquaticus, and generated a genome-wide linkage map for this species. Our map, composed of 117 markers, of which the majority are associated with genes known to be involved in pigmentation, eye, and appendage development, was used to identify loci of large effect responsible for several pigmentation traits and eye loss. Our study provides support for the prediction that significant morphological change can be mediated through one or a few genes. Surprisingly, we found that within population variability in eye size occurs through multiple mechanisms; eye loss has a different genetic basis than reduced eye size. Similarly, again within a population, the phenotype of albinism can be achieved by two different genetic pathways-either by a recessive genotype at one locus or doubly recessive genotypes at two other loci. Our work shows the potential of Asellus for studying the extremes of parallel and convergent evolution-spanning comparisons within populations to comparisons between vertebrate and arthropod systems.arthropods | regressive evolution | subterranean | mapping C ave animals have long interested biologists because of their bizarre and other-worldly appearance. Common characteristics of cave animals include the absence or great reduction of eyes, the elimination or near disappearance of pigmentation, and the elongation of limbs (1). These characteristics can be found in cave animals as diverse as salamanders, fish, spiders, shrimp, beetles, and collembolans. Most studies looking at the genetic basis of parallel or convergent evolution examine either closely related species with the same phenotypes or independently evolved populations of the same species with similar phenotypes (reviewed in ref.2). The cave system, however, is unique in that we can examine, and eventually compare, the genetic and molecular basis for the loss of eyes and pigmentation in vastly different (i.e., both invertebrate and vertebrate) taxa.A vertebrate cave fish, Astyanax mexicanus, has been established as an emerging model species for genetic and developmental analyses (reviewed in refs. 3 and 4). Mapping, using this species, has identified regions of the genome that are responsible for caveassociated morphological changes (5, 6). We decided to develop an invertebrate cave model that will provide an independent example of cave adaptation. Of the invertebrates, crustaceans have been particularly succ...

Molecular data show the enigmatic cave-dwelling diatomDiprora(Bacillariophyceae) to be a raphid diatom

“…Reduction of function in cave-dwelling organisms is well-known across a wide spectrum of organisms including arachnids (Jäger, 2001), crustaceans (Villacorta et al, 2008), insects (Juan & Emerson, 2010), fishes (Chakrabarty et al, 2012) and amphibians (Sket, 1997). In many of these cases, the mechanisms for the secondary loss of eyes and colouration are due to a loss of function in the cave environment (Culver et al, 1995;Porter & Crandall, 2003;Protas et al, 2011;Protas & Jeffery, 2012). The diatom Diadesmis gallica, which also can produce rapheless valves, is also known to occur in caves (Granetti, 1978;Cox, 2006a;Poulícková & Hašler, 2007).…”

Life in the Underworld: Anchialine cave biology in the era of speleogenomics

“…Furthermore, cave ecosystems present us with the opportunity to study organisms existing in habitats and conditions perhaps analogous to those of our planet many millions of years ago (Por, 2007). The special adaptations and evolutionary processes that gave rise to extant extremophiles, including some cave organisms, grant us the ability to examine questions regarding the origin and early evolution of life on our planet, and applications relating to these (i.e., astrobiology, Christin et al, 2010;Czyżewska, 2011;Gonzalez et al, 2011;Protas et al, 2011;Bonilla-Rosso et al, 2012). The unique processes and characteristics of anchialine caves (distribution, biogeochemistry and habitat stratification, chemosynthetic food-webs) and their biodiversity make them important communities to conserve in face of current anthropogenic threats (Myers et al, 2000;Iliffe, 2002;Porter, 2007;Mercado-Salas et al, 2013).…”

“…However, the scarcity of modern genomic methods being employed in the study of anchialine ecosystems remains to be addressed. Although biospeleological studies that incorporate genetic methodologies have been previously conducted (Adams & Humphreys, 1993;Porter, 2007;Page et al, 2008;Juan et al, 2010), the use of modern sequencing technologies for the study of anchialine caves still lags behind their freshwater and terrestrial counterparts (e.g., Friedrich et al, 2011;Protas et al, 2011;Friedrich, 2013;Gross et al, 2013), with perhaps the exception of some localized studies of specific taxa (e.g., Meland & Willassen, 2007;Russ et al, 2010;Neiber et al, 2012;von Reumont et al, 2014). In this contribution we examine the current state of knowledge on anchialine cave ecology, biodiversity, and evolution and also discuss the advantages and possibilities that biospeleological investigations at the genomic level, or "speleogenomics", will provide to the understanding of these fascinating systems -with special emphasis in the areas of biodiversity, phylogeography, and molecular evolution.…”

Phototransduction and clock gene expression in the troglobiont beetlePtomaphagus hirtusof Mammoth cave

“…Molecular studies of cave adaptation were pioneered in and have subsequently focused on the Mexican cave tetra Astyanax mexicanus (Jeffery, 2009). Very recently, this historical vertebrate bias has been alleviated by the molecular genetic analysis of eye and pigmentation loss in the waterlouse Asellus aquaticus (Protas et al, 2011). Both of these systems constitute dramatic examples of recent and fast evolution to the troglobiont state.…”