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Morphological convergence and adaptation in cave and pelagic scale worms (Polynoidae, Annelida).

ABSTRACT: Across Annelida, accessing the water column drives morphological and lifestyle modifications-yet in the primarily "benthic" scale worms, the ecological significance of swimming has largely been ignored. We investigated genetic, morphological and behavioural adaptations associated with swimming across Polynoidae, using mitogenomics and comparative methods. Mitochondrial genomes from cave and pelagic polynoids were highly similar, with non-significant rearrangements only present in cave Gesiella. Gene orders of the new mitogenomes were highly similar to shallow water species, suggestive of an underlying polynoid ground pattern. Being the first phylogenetic analyses to include the holopelagic Drieschia, we recovered this species nested among shallow water terminals, suggesting a shallow water ancestry. Based on these results, our phylogenetic reconstructions showed that swimming evolved independently three times in Polynoidae, involving convergent adaptations in morphology and motility patterns across the deep sea (Branchipolynoe), midwater (Drieschia) and anchialine caves (Pelagomacellicephala and Gesiella). Phylogenetic generalized least-squares (PGLS) analyses showed that holopelagic and anchialine cave species exhibit hypertrophy of the dorsal cirri, yet, these morphological modifications are achieved along different evolutionary pathways, i.e., elongation of the cirrophore versus style. Together, these findings suggest that a water column lifestyle elicits similar morphological adaptations, favouring bodies designed for drifting and sensing.

SUBMITTER: Gonzalez BC

PROVIDER: S-EPMC8139957 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Polynoidae Kinberg, 1856 has five branchiate genera: Branchipolynoe Pettibone, 1984, Branchinotogluma Pettibone, 1985, Branchiplicatus Pettibone, 1985, Peinaleopolynoe Desbruyères & Laubier, 1988, and Thermopolynoe Miura, 1994, all native to deep-sea, chemosynthetic-based habitats. Of these, Peinaleopolynoe has two accepted species; Peinaleopolynoe sillardi Desbruyères & Laubier, 1988 (Atlantic Ocean) and Peinaleopolynoe santacatalina Pettibone, 1993 (East Pacific Ocean). The goal of this study was to assess the phylogenetic position of Peinaleopolynoe, utilizing DNA sequences from a broad sampling of deep-sea polynoids. Representatives from all five branchiate genera were included, several species of which were sampled from near the type localities; Branchinotogluma sandersi Pettibone, 1985 from the Galápagos Rift (E/V "Nautilus"); Peinaleopolynoe sillardi from organic remains in the Atlantic Ocean; Peinaleopolynoe santacatalina from a whalefall off southern California (R/V "Western Flyer") and Thermopolynoe branchiata Miura, 1994 from Lau Back-Arc Basin in the western Pacific (R/V "Melville"). Phylogenetic analyses were conducted using mitochondrial (COI, 16S rRNA, and CytB) and nuclear (18S rRNA, 28S rRNA, and H3) genes. The analyses revealed four new Peinaleopolynoe species from the Pacific Ocean that are formally described here: Peinaleopolynoe orphanae Hatch & Rouse, sp. nov., type locality Pescadero Basin in the Gulf of California, Mexico (R/V "Western Flyer"); Peinaleopolynoe elvisi Hatch & Rouse, sp. nov. and Peinaleopolynoe goffrediae Hatch & Rouse, sp. nov., both with a type locality in Monterey Canyon off California (R/V "Western Flyer") and Peinaleopolynoe mineoi Hatch & Rouse, sp. nov. from Costa Rica methane seeps (R/V "Falkor"). In addition to DNA sequence data, the monophyly of Peinaleopolynoe is supported by the presence of ventral papillae on segments 12-15. The results also demonstrated the paraphyly of Branchinotogluma and Lepidonotopodium Pettibone, 1983 and taxonomic revision of these genera is required. We apply the subfamily name Lepidonotopodinae Pettibone 1983, for the clade comprised of Branchipolynoe, Branchinotogluma, Bathykurila, Branchiplicatus, Lepidonotopodium, Levensteiniella Pettibone, 1985, Thermopolynoe, and Peinaleopolynoe.

Project description:BackgroundMany cave-dwelling animal species display similar morphologies (troglomorphism) that have evolved convergent within and among lineages under the similar selective pressures imposed by cave habitats. Here we study such ecomorphological evolution in cave-dwelling Sclerobuninae harvestmen (Opiliones) from the western United States, providing general insights into morphological homoplasy, rates of morphological change, and the temporal context of cave evolution.Methodology/principal findingsWe gathered DNA sequence data from three independent gene regions, and combined these data with Bayesian hypothesis testing, morphometrics analysis, study of penis morphology, and relaxed molecular clock analyses. Using multivariate morphometric analysis, we find that phylogenetically unrelated taxa have convergently evolved troglomorphism; alternative phylogenetic hypotheses involving less morphological convergence are not supported by Bayesian hypothesis testing. In one instance, this morphology is found in specimens from a high-elevation stony debris habitat, suggesting that troglomorphism can evolve in non-cave habitats. We discovered a strong positive relationship between troglomorphy index and relative divergence time, making it possible to predict taxon age from morphology. Most of our time estimates for the origin of highly-troglomorphic cave forms predate the Pleistocene.Conclusions/significanceWhile several regions in the eastern and central United States are well-known hotspots for cave evolution, few modern phylogenetic studies have addressed the evolution of cave-obligate species in the western United States. Our integrative studies reveal the recurrent evolution of troglomorphism in a perhaps unexpected geographic region, at surprisingly deep time depths, and in sometimes surprising habitats. Because some newly discovered troglomorphic populations represent undescribed species, our findings stress the need for further biological exploration, integrative systematic research, and conservation efforts in western US cave habitats.

Project description:BACKGROUND:Bone-eating Osedax worms have proved to be surprisingly diverse and widespread. Including the initial description of this genus in 2004, five species that live at depths between 25 and 3,000 m in the eastern and western Pacific and in the north Atlantic have been named to date. Here, we provide molecular and morphological evidence for 12 additional evolutionary lineages from Monterey Bay, California. To assess their phylogenetic relationships and possible status as new undescribed species, we examined DNA sequences from two mitochondrial (COI and 16S rRNA) and three nuclear genes (H3, 18S and 28S rRNA). RESULTS:Phylogenetic analyses identified 17 distinct evolutionary lineages. Levels of sequence divergence among the undescribed lineages were similar to those found among the named species. The 17 lineages clustered into five well-supported clades that also differed for a number of key morphological traits. Attempts to determine the evolutionary age of Osedax depended on prior assumptions about nucleotide substitution rates. According to one scenario involving a molecular clock calibrated for shallow marine invertebrates, Osedax split from its siboglinid relatives about 45 million years ago when archeocete cetaceans first appeared and then diversified during the late Oligocene and early Miocene when toothed and baleen whales appeared. Alternatively, the use of a slower clock calibrated for deep-sea annelids suggested that Osedax split from its siboglinid relatives during the Cretaceous and began to diversify during the Early Paleocene, at least 20 million years before the origin of large marine mammals. CONCLUSION:To help resolve uncertainties about the evolutionary age of Osedax, we suggest that the fossilized bones from Cretaceous marine reptiles and late Oligocene cetaceans be examined for possible trace fossils left by Osedax roots. Regardless of the outcome, the present molecular evidence for strong phylogenetic concordance across five separate genes suggests that the undescribed Osedax lineages comprise evolutionarily significant units that have been separate from one another for many millions of years. These data coupled with ongoing morphological analyses provide a solid foundation for their future descriptions as new species.

Project description:During a visit to polychaete-rearing facilities in the vicinity of Bay of Cádiz (SW Iberian Peninsula, Atlantic Ocean), we sampled two populations of Marphysa (Annelida, Eunicidae) originally occurring at nearby intertidal soft bottoms, one being more than twice as long as the other at the same age. We analysed them using partial sequences of two mitochondrial genes, 16S rDNA and Cytochrome Oxidase I, and classical morphological observations. Our molecular results confirmed that the two populations corresponded to two different species, with PTP species delimitation values ranging from 0.973 (long-bodied species) to 0.999 (short-bodied species). Morphologically, the short-bodied species resembles the recently redescribed M. sanguinea (Montagu, 1813), but differs mainly in having some parapodia with two subacicular hooks (one bidentate and one unidentate) and three types of pectinate chaetae, Two isodont present all along the body, and one particularly large anodont asymmetric appearing only from mid-posterior parapodia. The long-bodied species resembles Marphysa aegypti Elgetany, El-Ghobashy, Ghoneim and Struck, 2018 both in size and in having very robust, unidentate subacicular hooks (single in most parapodia, two-both similar in size and form-in some posterior parapodia), but differs, among other features, in the maxillary formula, the number of acicula per parapodia and the number and shape of pectinate chaetae. Accordingly, we are here fully illustrating and formally describing the two Iberian populations as Marphysa gaditana sp. nov. (short-bodied) and Marphysa chirigota sp. nov. (long-bodied) and we are emending the description of M. aegypti based on our revision of the type material. Also, we discuss on the distribution of the species of the sanguinea-group and on the relevancy of taxonomically robust studies when dealing with species of commercial interest having the potential of being globally spread through human activities, as well as on the misunderstandings caused by the incorrect use of the "cosmopolitan species" concept.

Project description:BackgroundMany annelids, including well-studied species such as Platynereis, show similar structured segments along their body axis (homonomous segmentation). However, numerous annelid species diverge from this pattern and exhibit specialised segments or body regions (heteronomous segmentation). Recent phylogenomic studies and paleontological findings suggest that a heteronomous body architecture may represent an ancestral condition in Annelida. To better understand the segmentation within heteronomous species we describe the myogenesis and mesodermal delineation of segments in Siboglinum fiordicum during development.ResultsEmploying confocal and transmission electron microscopy we show that the somatic longitudinal musculature consists of four separate strands, among which ventrolateral one is the most prominent and is proposed to drive the search movements of the head of the late metatrochophore. The somatic circular musculature lies inside the longitudinal musculature and is predominantly developed at the anterior end of the competent larva to support the burrowing behaviour. Our application of transmission electron microscopy allows us to describe the developmental order of the non-muscular septa. The first septum to form is supported by thick bundles of longitudinal muscles and separates the body into an anterior and a posterior region. The second group of septa to develop further divides the posterior body region (opisthosoma) and is supported by developing circular muscles. At the late larval stage, a septum reinforced by circular muscles divides the anterior body region into a forepart and a trunk segment. The remaining septa and their circular muscles form one by one at the very posterior end of the opisthosoma.ConclusionsThe heteronomous Siboglinum lacks the strict anterior to posterior sequence of segment formation as it is found in the most studied annelid species. Instead, the first septum divides the body into two body regions before segments are laid down in first the posterior opisthosoma and then in the anterior body, respectively. Similar patterns of segment formation are described for the heteronomous chaetopterid Chaetopterus variopedatus and serpulid Hydroides elegans and may represent an adaptation of these annelids to the settlement and transition to the sedentarian-tubiculous mode of life.

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Morphological convergence and adaptation in cave and pelagic scale worms (Polynoidae, Annelida).

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