Assessing species boundaries in the open sea: an integrative taxonomic approach to the pteropod genus Diacavolinia

Abstract

To track changes in pelagic biodiversity in response to climate change, it is essential to accurately define species boundaries. Shelled pteropods are a group of holoplanktonic gastropods that have been proposed as bio-indicators because of their vulnerability to ocean acidification. A particularly suitable, yet challenging group for integrative taxonomy is the pteropod genus Diacavolinia, which has a circumglobal distribution and is the most species-rich pteropod genus, with 24 described species. We assessed species boundaries in this genus, with inferences based on geometric morphometric analyses of shell-shape variation, genetic (cytochrome c oxidase subunit I, 28S rDNA sequences) and geographic data. We found support for a total of 13 species worldwide, with observations of 706 museum and 263 freshly collected specimens across a global collection of material, including holo‐ and paratype specimens for 14 species. In the Atlantic Ocean, two species are well supported, in contrast to the eight currently described, and in the Indo‐Pacific we found a maximum of 11 species, partially merging 13 of the described species. Distributions of these revised species are congruent with well-known biogeographic provinces. Combining varied datasets in an integrative framework may be suitable for many diverse taxa and is an important first step to predicting species-specific responses to global change.

Resolving species boundaries in the Atlanta brunnea species group (Gastropoda, Pterotracheoidea)

“…These authors found at least 10 additional atlantid clades that may represent new species in addition to the 23 currently described present-day species. This study, as well as many others (Goetze 2010; Burridge et al 2015, 2019; Barco et al 2016; Bode et al 2017; Cornils et al 2017), highlights the importance of combining morphology (morphometrics), biogeography and molecular analyses when exploring species diversity in the open ocean.…”

Oceanic dispersal barriers in a holoplanktonic gastropod

“…Shell shape variation has also been shown to have a large genetic component, with heritabilities ranging between 0.36 and 0.71 in L. saxatilis (Conde-Padín et al, 2007) and between 0.16 and 0.56 in Nucella lapillus (Guerra-Varela et al, 2009). Furthermore, shell shape differences in conjunction with genetic differentiation have been used to identify species boundaries in different genera of holoplanktonic gastropods (Burridge et al, 2015(Burridge et al, , 2019Wall-Palmer et al, 2018) using an integrative species concept (McManus & Katz, 2009;Padial et al, 2010). Hence, strong reproductive isolation is probably involved in the maintenance of this primary dispersal barrier in the southern Atlantic gyre.…”

“…Shelled pteropods are especially vulnerable to global change, because of their thin aragonitic shells that are prone to dissolution (Bednaršek, Tarling, et al., 2012; Lischka et al., 2011; Manno et al., 2017), and they have been suggested as bioindicators of the effects of ocean acidification (Bednaršek, Klinger, et al., 2017). Several prior genetic studies on shelled pteropods have focused on resolving species boundaries via an integrative approach, combining genetic analyses and morphometric measurements of shells, to obtain a better understanding of species distribution patterns (Burridge et al., 2015, 2019; Shimizu et al., 2018). Other recent research efforts have addressed the response of shelled pteropods to acidified conditions to evaluate their acclimation to rapid increases in ocean acidity (Bednaršek, Feely, et al., 2017; Bogan et al., 2020; Maas et al., 2018; Moya et al., 2016).…”

Toward a global reference database of COI barcodes for marine zooplankton

“…These groups should be a priority for future DNA barcoding efforts, although challenges include lack of specimen vouchers due to poor preservation in ethanol. Recent studies have demonstrated the power of integrated molecular and morphometric analyses for these groups (Burridge et al 2015(Burridge et al , 2019Shimizu et al 2018;Choo et al 2020). Discovery of new species and increased estimates of global diversity can be expected, especially for species with widespread and multi-ocean distributions, which may be expected to reveal evidence of cryptic speciation.…”