Abstract

The use of planktonic foraminifera in paleoceanography requires taxonomic consistency and precise assessment of the species biogeography. Yet, ribosomal small subunit (SSUr) DNA analyses have revealed that most of the modern morpho-species of planktonic foraminifera are composed of a complex of several distinct genetic types that may correspond to cryptic or pseudo-cryptic species. These genetic types are usually delimitated using partial sequences located at the 3′end of the SSUrDNA, but typically based on empirical delimitation. Here, we first use patristic genetic distances calculated within and among genetic types of the most common morpho-species to show that intra-type and inter-type genetic distances within morpho-species may significantly overlap, suggesting that genetic types have been sometimes inconsistently defined. We further apply two quantitative and independent methods, ABGD (Automatic Barcode Gap Detection) and GMYC (General Mixed Yule Coalescent) to a dataset of published and newly obtained partial SSU rDNA for a more objective assessment of the species status of these genetic types. Results of these complementary approaches are highly congruent and lead to a molecular taxonomy that ranks 49 genetic types of planktonic foraminifera as genuine (pseudo)cryptic species. Our results advocate for a standardized sequencing procedure allowing homogenous delimitations of (pseudo)cryptic species. On the ground of this revised taxonomic framework, we finally provide an integrative taxonomy synthesizing geographic, ecological and morphological differentiations that can occur among the genuine (pseudo)cryptic species. Due to molecular, environmental or morphological data scarcities, many aspects of our proposed integrative taxonomy are not yet fully resolved. On the other hand, our study opens up the potential for a correct interpretation of environmental sequence datasets.

Highlights

  • Fossil shells of planktonic foraminifera constitute one of the most informative archive of biodiversity changes which are used as a proxy to reconstruct past ocean conditions [1]

  • Because species delimitations relying on genetic distances and/or phylogenetic analyses should be based on the same genetic marker to insure that they correspond to the same taxonomic level (e.g., [27,28]), SSU rDNA is still the most widely used marker for putative species delimitation in planktonic foraminifera

  • Intra-type distances are less variable than inter-type distances as their medians range from 0.21% (H. pelagica) to 3.2% (Truncorotalia truncatulinoides)

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Summary

Introduction

Fossil shells of planktonic foraminifera constitute one of the most informative archive of biodiversity changes which are used as a proxy to reconstruct past ocean conditions [1]. ITS rDNA barcodes are more commonly used than SSU rDNA to assess species-level diversity (e.g., [23,24]), foraminiferal ITS rDNA evolves at such fast rates that even sequences from closely related morpho-species cannot be aligned [22]. This characteristic is unusual in eukaryotes (e.g., [25,26]) and prevents the use of alignment methods involving sequences from different morpho-species. Molecular clocks and biogeographic patterns further suggested that these genetic types have been reproductively isolated for a significant amount of time and should be considered as cryptic or pseudo-cryptic species when subtle differences in shell morphology were detected [21,29,36,37,38]

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