Dating and biogeographical patterns in the sea slug genus Acanthodoris Gray, 1850 (Mollusca, Gastropoda, Nudibranchia)

Abstract

Recent studies investigating vicariance and dispersal have been focused on correlating major geological events with instances of taxonomic expansion by incorporating the fossil record with molecular clock analyses. However, this approach becomes problematic for soft-bodied organisms that are poorly represented in the fossil record. Here, we estimate the phylogenetic relationships of the nudibranch genus Acanthodoris Gray, 1850 using three molecular markers (16S, COI, H3), and then test two alternative geologically calibrated molecular clock scenarios in BEAST and their effect on ancestral area reconstruction (AAR) estimates employed in LAGRANGE. The global temperate distribution of Acanthodoris spans multiple geological barriers, including the Bering Strait (∼5.32 Mya) and the Baja Peninsula (∼5.5 Mya), both of which are used in our dating estimates. The expansion of the Atlantic Ocean (∼95-105 Mya) is also used to calibrate the relationship between A. falklandica Eliot, 1905 and A. planca Fahey and Valdés, 2005, which are distributed in southern Chile and South Africa respectively. Phylogenetic analyses recovered strong biogeographical signal and recovered two major clades representing northern and southern hemispheric distributions of Acanthodoris. When all three geological events are applied to the calibration analyses, the age for Acanthodoris is estimated to be mid-Cretaceous. When the expansion of the Atlantic Ocean is excluded from our analyses, however, Acanthodoris is estimated to be much younger, with a divergence time estimate during the Miocene. Regardless of divergence estimates, our AAR suggests that Acanthodoris may have origins in the Atlantic Ocean with the Atlantic acting as a dispersal point to the northeastern Pacific. These results suggest that Acanthodoris exhibits a rare instance of western trans-arctic expansion. This study also shows that northeast Pacific specimens of A. pilosa should be regarded as A. atrogriseata and that A. serpentinotus should be regarded as a synonym of A. pina.

Shallow water sea slugs (Gastropoda: Heterobranchia) from the northwestern coast of the Sea of Japan, north of Peter the Great Bay, Russia

“…5). Although the p-distance between these species is relatively low, lowered level of divergence is a characteristic for sibling species that descent during Pleistocene glaciations (Breslau, Valdés & Chichvarkhin, in press; Lindsay et al, 2016; Klienberger et al, 2016; Hallas, Simison & Gosliner, 2016). Likely, this phenomenon also occurs in amphiboreal species with direct development, e.g., Cadlina (Thompson, 1967) whose speciation took place during recent dispersal from a refugia.…”

Recalibrating the molecular clock for Arctic marine invertebrates based on DNA barcodes

“…Most previous studies have assumed the simultaneous divergence of sister taxa, ignoring differences in their environmental tolerances, ecological requirements, dispersal ability, and disregarding that biogeographic events will impact different ecological groups at different times (De Baets et al 2016). For example, most studies have assumed that the divergence of trans-Bering sister taxa coincided with the first opening of the Bering Strait (e.g., Hrincevich et al 2000;Wares and Cunningham 2001;Foltz et al 2008;Gérard et al 2008;Hallas et al 2016), ignoring the fact that its repeated opening and closure meant that multiple pulses of trans-Bering migrations are likely, a conclusion supported by the data (Carr 2010;Loeza-Quintana and Adamowicz 2018). If one repeats the calibration process in molluscs assuming simultaneous divergence during the major trans-Arctic interchange, the calibrated rate estimate would vary between 0.5%/MY and 6.1%/MY, depending upon which pair(s) is selected.…”

“…After exploring alternative calibration scenarios, it was apparent that the iterative calibration approach yielded results most concordant with the geological history of the Bering Strait. For example, the use of Bayesian analysis to calibrate a clock for the sister pair of Acanthodoris (Mollusca) dated their divergence at 5.32 Ma with the first opening of the Bering Strait (Hallas et al 2016). However, the inclusion of an additional calibration based on formation of the Baja Peninsula resulted in reducing the divergence time estimate to 2.4 Ma, with both estimates differing from the divergence time (1.2-1.4 Ma) estimated in this study.…”

A phylogeographic investigation of the kelp genusLaminaria(Laminariales, Phaeophyceae), with emphasis on the South Atlantic Ocean

“…() and Hallas et al. () also showed that the rockweed, Fucus , and the sea slug, Acanthodoris , respectively, could have invaded through the Bering Strait 3.5–5 mya.…”