Developmental Transcriptomic Analysis of the Cave-Dwelling Crustacean, Asellus aquaticus

Abstract

Cave animals are a fascinating group of species often demonstrating characteristics including reduced eyes and pigmentation, metabolic efficiency, and enhanced sensory systems. Asellus aquaticus, an isopod crustacean, is an emerging model for cave biology. Cave and surface forms of this species differ in many characteristics, including eye size, pigmentation, and antennal length. Existing resources for this species include a linkage map, mapped regions responsible for eye and pigmentation traits, sequenced adult transcriptomes, and comparative embryological descriptions of the surface and cave forms. Our ultimate goal is to identify genes and mutations responsible for the differences between the cave and surface forms. To advance this goal, we decided to use a transcriptomic approach. Because many of these changes first appear during embryonic development, we sequenced embryonic transcriptomes of cave, surface, and hybrid individuals at the stage when eyes and pigment become evident in the surface form. We generated a cave, a surface, a hybrid, and an integrated transcriptome to identify differentially expressed genes in the cave and surface forms. Additionally, we identified genes with allele-specific expression in hybrid individuals. These embryonic transcriptomes are an important resource to assist in our ultimate goal of determining the genetic underpinnings of the divergence between the cave and surface forms.

The genomics of phenotypically differentiated Asellusaquaticus cave, surface stream and lake ecotypes

“…Similar troglomorphic traits can also be found in A. aquaticus populations from Movile Cave in Romania (Turk et al, 1996), Molnar Janos Cave in Hungary (Pérez-Moreno et al, 2018) and Trebiciano Cave in Italy (Sket, 1994). Several studies using genetic and gene expression data mapped putative candidate genes associated with these traits in A. aquaticus (Gross et al, 2020;Mojaddidi et al, 2018;Protas et al, 2011;Stahl et al, 2015). To date, the only QTL mapping study using a cave vs. surface A. aquaticus intercross was performed by Protas et al, (2011), who identified loci that were associated with eye development and body pigmentation.…”

“…However, the study used a relatively small number of molecular markers, resulting in large confidence intervals for the detected QTL, often spanning half of the linkage group where the QTL were located and meaning candidate gene identification was not possible. Further, the transcriptomes of Slovenian and Hungarian cave and surface ecotypes have been sequenced (Gross et al, 2020;Pérez-Moreno et al, 2018;Stahl et al, 2015). Interestingly, Lürig et al, (2019) showed that body pigmentation in lake populations can be plastic and is highly dependent on diet (i.e., high vs. low nutrient availability associated with dark and light morphs, respectively.…”

Building on 150 Years of Knowledge: The Freshwater Isopod Asellus aquaticus as an Integrative Eco-Evolutionary Model System

“…Many of the morphological differences (e.g., pigmentation, eye size, and antennal article number) between cave and surface forms of A. aquaticus arise during embryonic development (Mojaddidi et al, 2018) and involve the differential expression of genes with diverse putative functions, such as phototransduction, photoreception, and eye development (Gross et al, 2019). Transcriptomic analyses of cave (versus surface) individuals also revealed allele-specific gene expression (Stahl et al, 2015;Gross et al, 2019), suggesting that cis-regulatory changes in gene expression may be responsible for phenotypic differences. Since cis-regulatory changes are known to constitute an important part of the genetic basis of adaptation (see Wray, 2007), A. aquaticus could provide insight into the contribution of cisregulatory changes to cave adaptation.…”

Into the Unknown: Microbial Communities in Caves, Their Role, and Potential Use

“…The dark, oligotrophic, and generally inhospitable environment of the most internal zone of the cave was for a long time perceived to be deprived of life forms. However, zoological and botanical studies showed over time a vast diversity of highly specialized lifeforms thriving inside various caves all over the world [22][23][24]. Furthermore, an interest in cave microbiome has been observed, as microorganisms isolated from these environments were revealed to have interesting properties in biotechnological, medical, and ecological sense [6,25,26].…”