Atlantic Oceanic Squids in the "Grey Speciation Zone"

Abstract

Cryptic species complexes represent an important challenge for the adequate characterization of Earth's biodiversity. Oceanic organisms tend to have greater unrecognized cryptic biodiversity since the marine realm was often considered to lack hard barriers to genetic exchange. Here, we tested the effect of several Atlantic and Mediterranean oceanic barriers on 16 morphospecies of oceanic squids of the orders Oegopsida and Bathyteuthida using three mitochondrial and one nuclear molecular marker and five species delimitation methods. Number of species recognized within each morphospecies differed among different markers and analyses, but we found strong evidence of cryptic biodiversity in at least four of the studied species (Chtenopteryx sicula, Chtenopteryx canariensis, Ancistrocheirus lesueurii, and Galiteuthis armata). There were highly geographically structured units within Helicocranchia navossae that could either represent recently diverged species or population structure. Although the species studied here can be considered relatively passive with respect to oceanic currents, cryptic speciation patterns showed few signs of being related to oceanic currents. We hypothesize that the bathymetry of the egg masses and duration of the paralarval stage might influence the geographic distribution of oceanic squids. Because the results of different markers and different species delimitation methods are inconsistent and because molecular data encompassing broad geographic sampling areas for oceanic squids are scarce and finding morphological diagnostic characters for early life stages is difficult, it is challenging to assess the species boundaries for many of these species. Thus, we consider many to be in the "grey speciation zone." As many oceanic squids have cosmopolitan distributions, new studies combining genomic and morphological information from specimens collected worldwide are needed to correctly assess the actual oceanic squid biodiversity.

Fig. 1

Summary of species delimitation analyses obtained with the cox1 database, depicted over the coalescent analyses obtained through BEAST 2.6.4 (Bouckaert et al. 2019). For convenience, clades formed by six or more sequences were collapsed. Numbers above branches refer to the node ages (Mya) and to the support of the node as the ultrafast bootstrap percentages (%) from the ML analysis and the posterior probabilities from the coalescent analysis, respectively. Bootstrap and posterior probabilities of <90% and 0.9, respectively, were not recorded. Dashes indicate a lack of support or clades with a different topology in the ML analysis. Asterisks designate clades that were set up as monophyletic for the coalescent analysis. Asterisks inside parenthesis designate lineages with one or more sequences coming from a locality close to the type locality of a nominal species. Vertical lines summarized the results from bPTP, ASAP, TCS, sGMYC, and mGMYC (see Supplementary Material and methods for more details). Numbers inside some results for delimitation analysis summarized the number of species found for a collapsed clade.