Subterranean Isopods Research Articles

Shedding light into Brazilian subterranean isopods (Isopoda, Oniscidea): expanding distribution data and describing new taxa

Shedding light into Brazilian subterranean isopods (Isopoda, Oniscidea): expanding distribution data and describing new taxa

Evolution of endoglucanase genes in subterranean and surface isopod crustaceans from Central Western Australia.

Recent studies have identified a significant number of endogenous cellulase genes in various arthropods, including isopods, allowing them to process hydrocarbons efficiently as a food source. While this research has provided insight into underlying gene-level processes in cellulose decomposition by arthropods, little is known about the existence and expression of cellulase genes in species from cave environments where carbohydrates are sparse. To investigate whether endogenous cellulase genes are maintained in subterranean species, we sequenced the transcriptomes of two subterranean paraplatyarthrid isopod species from calcrete (carbonate) aquifers of central Western Australia and a related surface isopod species. Seven protein-coding open-reading frames associated with endoglucanase genes were identified in all species. Orthology inference analyses, using a wide range of cellulase sequences from available databases, supported the endogenous origin of the putative endoglucanase genes. Selection analyses revealed that these genes are primarily subject to purifying selection in most of the sites for both surface and subterranean isopod species, indicating that they are likely to encode functional peptides. Furthermore, evolutionary branch models supported the hypothesis of an adaptive shift in selective pressure acting on the subterranean lineages compared with the ancestral lineage and surface species. Branch-site models also revealed a few amino acid sites on the subterranean branches to be under positive selection, suggesting the acquisition of novel adaptations to the subterranean environments. These findings also imply that hydrocarbons exist in subsurface aquifers, albeit at reduced levels, and have been utilized by subterranean isopods as a source of energy for millions of years.

Caecidotea burkensis, new species, a unique subterranean isopod from Burke’s Garden, with a synthesis of the biogeography and evolution of southwestern Virginia asellids

Caecidotea burkensis, a new species of subterranean asellid isopod, is described and illustrated from material collected from Lawson Cave, in Burke’s Garden, Tazewell County, Virginia. The type-locality in Burke’s Garden is located within the highest mountain basin in the southern Appalachians. Burke’s Garden is a unique, geologically isolated area encompassing one of the headwater streams of the New River basin. Phylogenetically, the isopod is a member of the forbesi Group, a clade comprised primarily of epigean species. The complex mountain valleys and coves of southwestern Virginia are an area of intense speciation among asellids that have produced a bizarre array of cavernicolous species belonging to groups of otherwise epigean isopods. In addition to a few subterranean species of the Caecidotea cannula and stygia Groups, the Lirceus hargeri Group possesses over a dozen species endemic to caves and springs in the region, mostly only now in the process of being discovered and described. With so much species richness, syntopy of two, or even three, asellid species is commonplace in caves and springs in southwestern Virginia.

Biogeographic history of subterranean isopods from groundwater calcrete islands in Western Australia

Groundwater calcretes in arid central Western Australia contain a diverse invertebrate groundwater fauna (stygofauna). Surveys have uncovered a diverse oniscidean isopod subterranean fauna above the water table (troglofauna), including species of a recently described genus Paraplatyarthrus. The aim of this study was to investigate the biogeographic history of Paraplatyarthrus and the timing of transitions from surface to subterranean habitats. Phylogenetic relationships among the isopod troglofauna from 11 groundwater calcretes along three palaeodrainage systems were assessed using one mitochondrial gene, cytochrome c oxidase subunit 1 (COI), and two nuclear markers, lysyl‐tRNA synthetase (LysRS) and 18S rRNA (18S) genes. Phylogenetic analyses revealed multiple sister lineage relationships between troglophile and troglobite lineages and evidence for divergent mtDNA lineages within species, providing a range of nodes for dating evolutionary transitions from surface to subterranean habitats. Relaxed molecular clock analyses provided evidence that evolutionary transitions from surface to subterranean environments took place between 13.3 and 1.75 million years ago, coinciding with the onset of aridification of Australia from the late Tertiary. In cases where groundwater calcretes contained multiple species, the taxa were not closely related phylogenetically, suggesting that these calcretes were independently colonised by multiple ancestral species. The study further confirmed the role of late/post‐Miocene aridification as a key driver of the evolution of subterranean invertebrates in the calcrete islands of Western Australia, supporting the climatic relict hypothesis. Troglobites most likely evolved from the troglophile ancestors that were capable of dispersal among, and active colonisation of, calcretes.

Less effective selection leads to larger genomes.

The evolutionary origin of the striking genome size variations found in eukaryotes remains enigmatic. The effective size of populations, by controlling selection efficacy, is expected to be a key parameter underlying genome size evolution. However, this hypothesis has proved difficult to investigate using empirical data sets. Here, we tested this hypothesis using 22 de novo transcriptomes and low-coverage genomes of asellid isopods, which represent 11 independent habitat shifts from surface water to resource-poor groundwater. We show that these habitat shifts are associated with higher transcriptome-wide . After ruling out the role of positive selection and pseudogenization, we show that these transcriptome-wide increases are the consequence of a reduction in selection efficacy imposed by the smaller effective population size of subterranean species. This reduction is paralleled by an important increase in genome size (25% increase on average), an increase also confirmed in subterranean decapods and mollusks. We also control for an adaptive impact of genome size on life history traits but find no correlation between body size, or growth rate, and genome size. We show instead that the independent increases in genome size measured in subterranean isopods are the direct consequence of increasing invasion rates by repeat elements, which are less efficiently purged out by purifying selection. Contrary to selection efficacy, polymorphism is not correlated to genome size. We propose that recent demographic fluctuations and the difficulty of observing polymorphism variation in polymorphism-poor species can obfuscate the link between effective population size and genome size when polymorphism data are used alone.

No Evidence That Nitrogen Limitation Influences the Elemental Composition of Isopod Transcriptomes and Proteomes.

The field of stoichiogenomics aims at understanding the influence of nutrient limitations on the elemental composition of the genome, transcriptome, and proteome. The 20 amino acids and the 4 nt differ in the number of nutrients they contain, such as nitrogen (N). Thus, N limitation shall theoretically select for changes in the composition of proteins or RNAs through preferential use of N-poor amino acids or nucleotides, which will decrease the N-budget of an organism. While these N-saving mechanisms have been evidenced in microorganisms, they remain controversial in multicellular eukaryotes. In this study, we used 13 surface and subterranean isopod species pairs that face strongly contrasted N limitations, either in terms of quantity or quality. We combined in situ nutrient quantification and transcriptome sequencing to test if N limitation selected for N-savings through changes in the expression and composition of the transcriptome and proteome. No evidence of N-savings was found in the total N-budget of transcriptomes or proteomes or in the average protein N-cost. Nevertheless, subterranean species evolving in N-depleted habitats displayed lower N-usage at their third codon positions. To test if this convergent compositional change was driven by natural selection, we developed a method to detect the strand-asymmetric signature that stoichiogenomic selection should leave in the substitution pattern. No such signature was evidenced, indicating that the observed stoichiogenomic-like patterns were attributable to nonadaptive processes. The absence of stoichiogenomic signal despite strong N limitation within a powerful phylogenetic framework casts doubt on the existence of stoichiogenomic mechanisms in metazoans.

Molting and cuticle deposition in the subterranean trichoniscid Titanethes albus (Crustacea, Isopoda)

Terrestrial isopods are a suitable group for the study of cuticle synthesis and calcium dynamics because they molt frequently and have evolved means to store calcium during molt. Little data is currently available on molting in Synocheta and subterranean isopods. We studied the molting dynamics in the subterranean trichoniscid Titanethes albus under laboratory conditions and performed a microscopic investigation of sternal CaCO3 deposits and the tergal epithelium during molt in this species. In accordance with its lower metabolic rate, molting in the laboratory is roughly 2–3 times less frequent in Titanethes albus than would be expected for an epigean isopod under similar conditions. Animals assumed characteristic postures following the molt of each body half and did not consume the posterior exuviae after posterior molt. The structure of sternal calcium deposits and the ultrastructural characteristics of the epidermis during cuticle formation in Titanethes albus are similar to those described in representatives of Ligiidae. During the deposition of the exocuticle, the apical plasma membrane of epidermal cells forms finger-like extensions and numerous invaginations. In the ecdysial space of individuals in late premolt we observed cellular extensions surrounded by bundles of tubules.

Evolutionary biogeography of the Microparasellid isopod Microcharon (Crustacea) in the Mediterranean Basin

The interstitial subterranean isopod Microcharon (Crustacea) is highly diversified within the Mediterranean. The present distribution of 70 species is considered the result of the joint history of this genus and its environment. This stygobiont is derived from marine surface ancestors. Both Plate Tectonics and the two-step model of colonization and evolution, the second phase of which represents vicariance during the Tethys regressions, enable an understanding of the evolutionary history of this monophyletic group. The single extant marine littoral species was separated from its sister group by the closure of the Gibraltar Straits during the Messinian. The drift of the Apulian plate, the Alboran-Kabylian-Calabrian fragment as well as the opening of the western Mediterranean through the translation of the Corsican-Sardinia plate could explain the divergences in the western and the eastern Mediterranean. The primitive sister groups in Morocco and in Spain would have been left by the Turonian Tethys regression. Such regressions of the Tethys embayments could have played a major role in the evolution of the genus from Turanian up to Tortonian in Norht Africa, and up to Pliocene and even to Pleistocene in Italian, Iberian and Greek zones. Several eastern European species may be a product of the Paratethys regressions. Everywhere, species with plesiomorphic characters are related to old regressions and vice versa. Local geological events could have resulted in further vicariance divergences. There is a good congruence between the evolutionary history of Microcharon and other stygobiont isopod, amphipods or syncarids living in the same regions studied in the Mediterranean.

Stygobromus canadensis, a new subterranean amphipod crustacean (Crangonyctidae) from Canada, with remarks on Wisconsin refugia

Stygobromus canadensis, new species, is described from Castleguard Cave, a large alpine cave located in the Canadian Rockies of Alberta. This is the first subterranean amphipod crustacean reported from Canada and the ninth member of the genus found north of the southern limits of Pleistocene glaciation. Considering the evidence against postglacial dispersal (e.g., endemicity and lack of close affinity with species living farther south), and the presence of a subterranean isopod in the same cave, it is hypothesized that these small aquatic crustaceans survived the Wisconsin glaciers in deep, groundwater refugia under the ice. There is some evidence to suggest that Castleguard Cave, itself, could have served as such a refugium.

Occurrence of Subterranean Isopods in Epigean Waters

Occurrence of Subterranean Isopods in Epigean Waters

Differential Growth and Evolution in a Subterranean Isopod

(1) Measurements were made of body length, width and the lengths of antennae, head, thorax, pleotelson and parts of the uropod of twenty-six specimens of Asellus californicus ranging in size from 1.5 by 0.3 mm to 11.1 by 1.7 mm in order to obtain a quantitative picture of differential growth in this subterranean isopod. (2) The data obtained were analyzed and found to conform with Huxley's law of heterogonic growth, using body width as the standard of comparison. (3) The differential growth ratio (k) for each structure was not uniform overthe entire range of observation but increased abruptly at the middle of the range, dividing the period of growth studied into two uniform stanzas. The constants in the heterogony formula were calculated separately for each structure for the two stanzas, as well as for the entire range when the change from first to second stanza was slight or not statistically significant. (4) Within the range of body width 0.3 to 1.0 mm, growth in length is practically isogonic for all structures except the pleotelson and the uropod, which is heterogonic, due to the marked heterogony in its basal segment. (5) In the second stanza (body width of 1.0 to 1.7 mm) there is a simultaneous and significant onset of heterogony in all structures, with the possible exception of the thorax, although in some eases the increase in the value of k from first to second stanza is not significant. Extreme heterogony is exhibited by the protopodite and endopodite of the uropod with k values of 3.8 and 3.3, respectively. (6) Heterogony is not exhibited to the same degree in all structures or parts and the visible consequences of differences in the growth coefficient, k, are described in terms of changing proportions of parts with growth. The best example is the uropod, in which, as a result of different degrees of heterogony in the protopodite and endopodite and the practically isogonic growth of the exopodite, the proportionate lengths of protopodite, endopodite and exopodite change from about 4:6:5, respectively, in the smallest specimens to about 6.4.1 in the largest. (7) The growth gradient in the longitudinal axis of the body shows, in the first stanza, a center of differential growth in the protopodite of the ufopod from which the gradient slopes down proximally to the head and distally to the endopodite. In the second stanza, the growth gradient features two terminal centers of high d ifferential growth, the second antenna and again the protopodite which is now an extremely high center. From these two distal centers, the growth gradient slopes down sharply to the middle of the body. The whole gradient in the second stanza is significantly elevated above the level line of isogonic growth. (8) Rate genes affecting the various parts of the body and possibly the body as a whole are suggested as the cause of disproportionate but orderly growth. That the heterogony of the second stanza may be a male secondary sexual or sex-limited character is a strong possibility. Reasons are given to show that functional hypertrophy is an inadequate explanation for the extreme heterogony of the second antennae and uropods. (9) The taxonomic and evolutionary significance of heterogonic elongation is discussed. Relative elongation is shown to have no systematic value in separating the subterranean isopods as a genus (Caecidotea) from the surface forms not only because it is a convergent character but also because it is not even a constant specific character, since relative elongation varies with age in individuals of a species as a result of heterogony. Other reasons for invalidating this unnatural genus are reviewed. The elongation distinguishing subterranean forms from surface species possibly resulted in consequence of parallel mutations of rate genes in the ancestral surface species. If so, the mutant genes express themselves relatively late in our Asellus californicus. The heterogonic elongation of parts in this subterranean isopod results in a recapitulation of ancestral body proportions.

A new subterranean isopod from Kansas

A new subterranean isopod from Kansas

On a new and peculiar freshwater isopod from Mount Kosciusko

Towards the end of 1889 I received from the Trustees of the Australian Museum, Sydney, a small collection of Australian Crustacea, containing among others, some terrestrial and freshwater species collected by Mr. R. Helms while on an expedition to Mount Kosciusko on behalf of the Museum. Among these I at once saw that one was quite different from any of the terrestrial and fresh-water Crustacea previously described from Australia, and that it belonged to a genus Phreatoicus established by myself in 1882, for a peculiar blind subterranean Isopod found in wells in Canterbury, New Zealand. This genus was of special interest both because of the situation in which the original species was found, and because it combined characters belonging to several different families, and was also, to some extent, intermediate between the Isopoda and the Amphipoda The discovery of a species belonging to the same genus in such a widely remote situation as Mount Kosciusko, and living under such different conditions is therefore of peculiar interest,