Diverse marine fish and squid form symbiotic associations with extracellular bioluminescent bacteria. These symbionts are typically free-living bacteria with large genomes, but one known lineage of symbionts has undergone genomic reduction and evolution of host dependence. It is not known why distinct evolutionary trajectories have occurred among different luminous symbionts, and not all known lineages previously had genome sequences available. In order to better understand patterns of evolution across diverse bioluminescent symbionts, we de novo sequenced the genomes of bacteria from a poorly studied interaction, the extracellular symbionts from the “lures” of deep-sea ceratioid anglerfishes. Deep-sea anglerfish symbiont genomes are reduced in size by about 50% compared to free-living relatives. They show a striking convergence of genome reduction and loss of metabolic capabilities with a distinct lineage of obligately host-dependent luminous symbionts. These losses include reductions in amino acid synthesis pathways and abilities to utilize diverse sugars. However, the symbiont genomes have retained a number of categories of genes predicted to be useful only outside the host, such as those involved in chemotaxis and motility, suggesting that they may persist in the environment. These genomes contain very high numbers of pseudogenes and show massive expansions of transposable elements, with transposases accounting for 28 and 31% of coding sequences in the symbiont genomes. Transposon expansions appear to have occurred at different times in each symbiont lineage, indicating either independent evolutions of reduction or symbiont replacement. These results suggest ongoing genomic reduction in extracellular luminous symbionts that is facilitated by transposon proliferations.
During a two year population ecology study in a cave environment, 15 Eurycea (ZTyphlotriton) spelaea were observed ingesting bat guano. Furthermore, E. spelaea capture numbers increased significantly during the time that grey bats (Myotis grisescens) deposited fresh guano. We investigated the hypothesis that this behaviour was not incidental to the capture of invertebrate prey, but a diet switch to an energy-rich detritus in an oligotrophic environment. Stable isotope assays determined that guano may be assimilated into salamander muscle tissue, and nutritional analyses revealed that guano is a comparable food source to potential invertebrate prey items. This is the first report of coprophagy in a salamander and in any amphibian for reasons other than intestinal inoculation. Because many temperate subterranean environments are often energy poor and this limitation is thought to select for increased diet breadth, we predict that coprophagy may be common in subterranean vertebrates where it is not currently recognized.
The interdependence of diverse organisms through symbiosis reaches even the deepest parts of the oceans. As part of the DEEPEND project (deependconsortium.org) research on deep Gulf of Mexico biodiversity, we profiled the bacterial communities (‘microbiomes’) and luminous symbionts of 36 specimens of adult and larval deep-sea anglerfishes of the suborder Ceratioidei using 16S rDNA. Transmission electron microscopy was used to characterize the location of symbionts in adult light organs (esca). Whole larval microbiomes, and adult skin and gut microbiomes, were dominated by bacteria in the genera Moritella and Pseudoalteromonas. 16S rDNA sequencing results from adult fishes corroborate the previously published identity of ceratioid bioluminescent symbionts and support the findings that these symbionts do not consistently exhibit host specificity at the host family level. Bioluminescent symbiont amplicon sequence variants were absent from larval ceratioid samples, but were found at all depths in the seawater, with a highest abundance found at mesopelagic depths. As adults spend the majority of their lives in the meso- and bathypelagic zones, the trend in symbiont abundance is consistent with their life history. These findings support the hypothesis that bioluminescent symbionts are not present throughout host development, and that ceratioids acquire their bioluminescent symbionts from the environment.
Deep-sea anglerfishes are relatively abundant and diverse, but their luminescent bacterial symbionts remain enigmatic. The genomes of two symbiont species have qualities common to vertically transmitted, host-dependent bacteria. However, a number of traits suggest that these symbionts may be environmentally acquired. To determine how anglerfish symbionts are transmitted, we analyzed bacteria-host codivergence across six diverse anglerfish genera. Most of the anglerfish species surveyed shared a common species of symbiont. Only one other symbiont species was found, which had a specific relationship with one anglerfish species, Cryptopsaras couesii. Host and symbiont phylogenies lacked congruence, and there was no statistical support for codivergence broadly. We also recovered symbiont-specific gene sequences from water collected near hosts, suggesting environmental persistence of symbionts. Based on these results we conclude that diverse anglerfishes share symbionts that are acquired from the environment, and that these bacteria have undergone extreme genome reduction although they are not vertically transmitted.
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Mosaic evolution refers to the pattern whereby different organismal traits exhibit differential rates of evolution typically due to reduced levels of trait covariation through deep time (i.e., modularity). These differences in rates can be attributed to variation in responses to selective pressures between individual traits. Differential responses to selective pressures also have the potential to facilitate functional specialization, allowing certain traits to track environmental stimuli more closely than others. The teleost skull is a multifunctional structure comprising a complex network of bones and thus an excellent system for which to study mosaic evolution. Here we construct an ultrametric phylogeny for a clade of Neotropical electric fishes (Apteronotidae: Gymnotiformes) and use three-dimensional geometric morphometrics to investigate patterns of mosaic evolution in the skull and jaws. We find strong support for a developmental, three-module hypothesis that consists of the face, braincase, and mandible, and we find that the mandible has evolved four times faster than its neighboring modules. We hypothesize that the functional specialization of the mandible in this group of fishes has allowed it to outpace the face and braincase and evolve in a more decoupled manner. We also hypothesize that this pattern of mosaicism may be widespread across other clades of teleost fishes.
Here we review the thirty year recovery effort and conservation status of the Ozark cavefish, Amblyopsis rosae. We summarized the historic and current range of the species, and report county range extensions for both A. rosae and its confamilial Typhlichthys subterraneus. Ozark cavefish survey data spanning almost a century were analyzed for temporal trends using the Mann-Kendall Test/Sen's Slope Estimator Method. Results were inconclusive because variance was high and the majority of data sets were not sufficiently large to detect a trend. However, the two largest populations (Cave Springs Cave and Logan Cave, Benton Co., Arkansas) have stabilizing or increasing survey counts. While the number of active cavefish sites has decreased over 50% since 1990, the number of surveyed individuals has not. Reasons for endangerment were reanalyzed since federal listing; the primary threat has shifted from overcollection to habitat degradation. We analyzed the progress of recovery task implementation, and we critically evaluated the basis of delisting criteria. Recovery Task 1, the hydrogeologic delineation of subterranean habitats, is almost complete. Recovery Task 2 prescribes protection and management for Recovery Caves, and important progress has been made. Recovery Task 3 involves the development and implementation of monitoring programs in Recovery Caves. Several important studies have been performed, and indicate that many cavefish populations are experiencing chronic, low-level exposure to a suite of anthropogenic contaminants. Delisting conditions are largely unattainable as currently worded. We suggest that recovery criteria be amended such that habitat protection goals are attainable, that the list of Recovery Caves can be periodically updated, and that the recovery Environ Biol Fish (2010) 87:55-88 population goal is increased and distributed between more sites.
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