Foraminifera

Syst. Biol.
65(5):925–940, 2016
© The Author(s) 2016. Published by Oxford University Press, on behalf of the Society of Systematic Biologists. All rights reserved.
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DOI:10.1093/sysbio/syw031
Advance Access publication April 12, 2016
Nomenclature for the Nameless: A Proposal for an Integrative Molecular Taxonomy of

Cryptic Diversity Exemplified by Planktonic Foraminifera
R APHAËL MORARD1,∗ , GILLES ESCARGUEL2 , AGNES K. M. WEINER1,3 , AURORE ANDRÉ4 , CHRISTOPHE J. DOUADY2,5 ,
CHRISTOPHER M. WADE6 , KATE F. DARLING7,8 , YURIKA UJIIÉ9 , HEIDI A. SEEARS10 , FRÉDÉRIC QUILLÉVÉRÉ11 ,
THIBAULT DE GARIDEL-THORON12 , COLOMBAN DE VARGAS13,14 , AND MICHAL KUCERA1
1 MARUM Center for Marine Environmental Sciences, University of Bremen, Leobener Strasse, 28359 Bremen, Germany, 2 Université de Lyon; UMR5023
Ecologie des Hydrosystémes Naturels et Anthropisés; Universiteì Lyon 1; ENTPE; CNRS; 6 rue Raphaël Dubois, 69622 Villeurbanne, France,
3 Japan Agency for Marine Earth Science and Technology (JAMSTEC), 2-15 Natsushima-cho, Yokosuka 237-0061, Kanagawa, Japan, 4 Université de
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Reims-Champagne-Ardenne, UFR Sciences Exactes et Naturelles, Campus Moulin de la Housse, Batiment 18, 51100 REIMS, France, 5 Institut Universitaire
de France, 103 Boulevard Saint-Michel, 75005 Paris, France, 6 School of Life Sciences, University of Nottingham, University Park, Nottingham NG7 2RD,
UK, 7 School of GeoSciences, University of Edinburgh, Edinburgh EH9 3JW, UK, 8 School of Geography and GeoSciences, University of St Andrews, Fife
KY16 9AL, UK, 9 Department of Biology, Shinshu University, Asahi3-1-1, Matsumoto, Nagano 390-8621, Japan, 10 Department of Biology, Gilmer Hall,
University of Virginia, 485 McCormick Road, Charlottesville, VA 22904, USA, 11 Univ Lyon, Université Lyon 1, ENS de Lyon, CNRS, UMR 5276 LGL-TPE,
F-69622 Villeurbanne, France; 12 Centre Européen de Recherche et d’Enseignement de Géosciences de l’Environnement, Centre National de la Recherche
Scientifique, et Aix-Marseille Université, Aix-en-Provence, France, 13 Centre National de la Recherche Scientifique, UMR 7144, EPEP, Station Biologique de
Roscoff, 29680 Roscoff, France, and 14 Sorbonne Universités, UPMC Univ Paris 06, UMR 7144, Station Biologique de Roscoff, 29680 Roscoff, France
∗ Correspondence to be sent to: MARUM Center for Marine Environmental Sciences, University of Bremen, Leobener Strasse, 28359 Bremen, Germany;
E-mail: rmorard@marum.de.
Received 1 October 2015; reviews returned 1 December 2015; accepted 4 April 2016
Associate Editor: Adrian Paterson
Abstract.—Investigations of biodiversity, biogeography, and ecological processes rely on the identification of “species” as
biologically significant, natural units of evolution. In this context, morphotaxonomy only provides an adequate level of
resolution if reproductive isolation matches morphological divergence. In many groups of organisms, morphologically
defined species often disguise considerable genetic diversity, which may be indicative of the existence of cryptic species.
The diversity hidden by morphological species can be disentangled through genetic surveys, which also provide access
to data on the ecological distribution of genetically circumscribed units. These units can be identified by unique DNA
sequence motifs and allow studies of evolutionary and ecological processes at different levels of divergence. However, the
nomenclature of genetically circumscribed units within morphological species is not regulated and lacks stability. This
represents a major obstacle to efforts to synthesize and communicate data on genetic diversity for multiple stakeholders. We
have been confronted with such an obstacle in our work on planktonic foraminifera, where the stakeholder community is
particularly diverse, involving geochemists, paleoceanographers, paleontologists, and biologists, and the lack of stable
nomenclature beyond the level of formal morphospecies prevents effective transfer of knowledge. To circumvent this
problem, we have designed a stable, reproducible, and flexible nomenclature system for genetically circumscribed units,
analogous to the principles of a formal nomenclature system. Our system is based on the definition of unique DNA sequence
motifs collocated within an individual, their typification (in analogy with holotypes), utilization of their hierarchical
phylogenetic structure to define levels of divergence below that of the morphospecies, and a set of nomenclature rules
assuring stability. The resulting molecular operational taxonomic units remain outside the domain of current nomenclature
codes, but are linked to formal morphospecies as regulated by the codes. Subsequently, we show how this system can be
applied to classify genetically defined units using the SSU rDNA marker in planktonic foraminifera and we highlight
its potential use for other groups of organisms where similarly high levels of connectivity between molecular and
formal taxonomies can be achieved. [Cryptic species; genetic diversity; planktonic foraminifera; molecular nomenclature;
MOTUs.]
biogeography, ecology, and conservation biology. Over

The Lack of Formal Taxonomy for Molecular Diversity
the last 250 years, a large and still growing body
For over two centuries, formalized and codified of taxonomic knowledge has been created, allowing
nomenclature has been the cornerstone of biological scientists to synthesize data accumulated by generations
research. By using simple and efficient rules for the of taxonomists across the globe (Puillandre et al. 2012a).
classification of organisms into hierarchically structured Current codes for biological nomenclature (ICZN
units, Linnean systematics provided biologists with 1999; ICN 2011; ICTV 2011; Garrity et al. 2015) require
a common language for taxa and their names. As that each species must be associated with a formal
a consequence, the results of fundamental taxonomic description, but they do not specify the nature of
research (description of taxa) could be applied characters on which the description is to be based.
in other disciplines such as evolutionary biology, Thus, in theory, there is nothing that speaks against the
925
926 SYSTEMATIC BIOLOGY VOL. 65
practice to describe species by molecular evidence alone MOTUs prevents a deeper understanding of speciation
(Jörger and Schrödl 2013). Nevertheless, such practice processes, biogeography, and ecological interactions at
bears the risk of creating a parallel taxonomical universe the level of cryptic species.
detached from the existing body of knowledge (mostly The modalities for the development of an integrative
based on morphological features) and associated with framework to include DNA sequence motifs into taxa
a potentially large instability of species delimitation. It delimitation are currently hotly debated in the literature
would also isolate the nomenclature of extant species (Padial et al. 2010; Carstens et al. 2013; Miralles and
from fossils, and render the recognition of such entities Vences 2013; Leliaert et al. 2014; Pante et al. 2014; Flot
dependent on access to molecular data. Even in an 2015), fueled by the advent of massive environmental
age of cheap-and-easy molecular analyses, it remains sequencing surveys (e. g., Logares et al. 2014; de Vargas
essential to allow quick and efficient classification and et al. 2015). Much effort has been directed toward the
identification of extant or fossil organisms on the basis of evaluation of methods and concepts to delimit entities
field observations. Therefore, most species descriptions by molecular markers (Satler et al. 2013; Leavitt et al.
rely on phenotypic characters. Despite its practical value 2015) and toward the stability of the boundaries of the
and stability, the traditional de facto phenotypically based circumscribed MOTUs (Carstens et al. 2013). In contrast,

taxonomy is challenged by the discovery that molecular there have been few if any attempts to deal with the
data often provide greater taxonomic resolution than nomenclature of the resulting units (Caron 2013). The
morphology (Bickford et al. 2007). The existence of current practice is to design for each study an ad hoc
cryptic (i.e., phenotypically unseen) species by itself does classification scheme with arbitrary labels and levels,
not question the validity of the current formal taxonomy. which are often not conserved across studies (Pante et al.
It does, however, affect the biological interpretation of 2015).
phenotypically defined species and it implies that even In summary, the advent of molecular ecology has
for extant species, phenotypic taxonomy will never be added a layer of cryptic diversity to the classically
comprehensive at the level of biological (reproductive) described morphospecies. MOTUs often correspond
species. better to biological (reproductive) species concepts
A common alternative is to use a transitional (Amato et al. 2007) than morphologically defined OTUs,
system pending formal taxonomy by defining molecular providing more appropriate units to assess ecological
operational taxonomic units (MOTUs) using DNA-based and evolutionary hypotheses and concepts. However,
automatic delimitation (Flot 2015). However, unless no attempt has been made to provide a nomenclature
such MOTUs are treated as formal taxa as for the system for them, an unescapable formal prerequisite
MArine STramenopiles “MAST” which have been first to provide a common language for discussion across
described from SSU rDNA sequencing (Massana et al. disciplines and novel data sets. Such a system should
2004), no formal rules regulate their denomination. be able to name MOTUs below the level of the
The PhyloCode has been proposed as an alternative morphospecies and should meet the criteria of an
to the Linnean system to name phylogenetic clades interim taxonomic system: uniqueness of the names
(de Queiroz and Cantino 2001) but it provides names employed, stability, and a proper definition of the given
to ranks above the species level and is therefore not ranks (Schindel and Miller 2009). This system should
suitable for a nomenclature of cryptic species. The be employed when the Linnean system is impractical or
Barcoding Index Number (BIN) system (Ratnasingham cannot be used. It has to provide for regular revision and
and Hebert 2013) has been proposed to register all integrate novel concepts in molecular taxonomy and/or
entries in the Barcode of Life Data (BOLD) system automated delimitation. Finally, it should facilitate the
portal (Ratnasingham and Hebert 2007). The BIN system transfer of a given MOTU from this interim system to
is meant to resolve to the biological species level the formal nomenclature, as soon as it is diagnosed with
and has been conceived to avoid synonymy in the morphological characteristics as recently exemplified
BOLD portal. It goes some way toward stabilization with copepods (Karanovic et al. 2016).
of names and disambiguation of conflict, but because In attempting to export the knowledge of molecular
the system only classifies species it lacks a hierarchical ecology of extant planktonic foraminifera to their
structure and shares the limitations incurred by using fossil record, we have been repeatedly confronted
a universal barcode marker. At present, none of the with both major impediments resulting from the
existing systems can effectively incorporate multiple lack of MOTU nomenclature: stability and transfer.
hierarchies of MOTUs nested below the level of formally The spatial and ecological distributions of cryptic
described species. As a result, contrary to taxa in the species of extant planktonic foraminifera are narrower
current formal nomenclature, it is difficult to discuss compared with the range of their morphospecies and the
accurately the identity, occurrence, and properties of information on their present diversity and distribution
MOTUs, including potential cryptic species (Pante et al. could improve the accuracy of paleoceanographic
2014). Cryptic species, even when detected, often remain reconstruction (Kucera and Darling 2002; Morard et al.
nameless. Lack of stable names of MOTUs impedes 2013). Benefiting from the existence of a comprehensive
transfer of knowledge across disciplines. As a result, morphological taxonomy of this group linked through
MOTUs are often excluded from conservation research single-cell ribosomal DNA sequencing surveys to genetic
and efforts and the lack of a stable nomenclature of diversity (Morard et al. 2015), we are now in the position
2016 POINTS OF VIEW 927
to propose a simple, robust, and efficient nomenclature of a small subset of informative loci (Amato et al.
system that gives stable names (labels) to MOTUs, 2007). Ultimately, this procedure is the basis of the
and links them to the formal nomenclature without barcoding concept (Hebert et al. 2003), cataloging
compromising its rules. The purpose of this article is unique sequence patterns from a given informative
to describe and explain the design of the system, show “barcode” region. Although practical in its application,
how it can be applied to foraminifera, and highlight its this approach has been criticized (e.g., Taylor and
potential for taxa with a similar degree and structure of Harris 2012), because of the differences that may exist
cryptic diversity. between gene trees and species trees. As a result, recent
barcoding initiatives proposed the use of multiple loci
(Pawlowski et al. 2012). The use of multilocus sequence
data represents a balanced alternative combining
the advantages of barcoding with a higher level of
FROM A UNIFIED SPECIES CONCEPT TO A FORMAL
representativeness: allowing the investigation of both
NOMENCLATURE SYSTEM FOR MOTUS population genetics and cryptic speciation (e.g., Salerno
Since Mayr (1942), species are viewed as groups et al. 2015).

of actually or potentially interbreeding organisms, Notwithstanding the choice of approach or marker
which are reproductively isolated from each other. selection, automated methods for MOTU boundary
When integrated over generations, such reproductively delineation have been developed to avoid arbitrary
defined groups constitute evolutionary lineages sensu thresholds or subjective interpretation of phylogenetic
Simpson (1961), that is, ancestor-descendant lineages trees. Such methods assume that the sequence
of organisms evolving conjointly on the hereditary divergence can be partitioned between divergence due
ground. de Queiroz (2007) advocated a unified species to reproductive isolation and variation occurring within
concept where species are treated as separately a population, attempting to define MOTUs such that
evolving metapopulation lineages, making their mutual they best correspond to species sensu de Queiroz (2007).
separation and unique evolutionary history the only These methods can be based on single or multilocus
criteria necessary to justify their recognition. When information. They either exploit a barcode gap (e.g.,
applied to living organisms, this concept treats species Puillandre et al. 2012b) or detect the boundary between
as snapshots in time of such metapopulation lineages. population signal and divergence reflecting species
During their evolution, metapopulation lineages branching by coalescent statistics (e.g., Pons et al. 2006),
acquire secondary properties (phenetic traits, different by mutual allelic exclusivity (Flot et al. 2010), or model
ecological niches, reciprocal monophyly, reproductive speciation in terms of numbers of substitutions (Zhang
incompatibility, etc.) that differentiate them from other, et al. 2013). In the same way as taxonomists empirically
more or less distantly related metapopulation lineages. do, some methods tend to lump, while others tend to
In the course of this process they first occupy a “gray split taxa (Miralles and Vences 2013; André et al. 2014;
zone” where the species delimitation under different Fig. 1c). Splitting and lumping both bear advantages
criteria may be ambiguous and only later reach a state and caveats; overall, there are so many combinations
of unambiguous separation (Fig. 1 in de Queiroz 2007). of parameters that may be relevant to delineate species
Thus, the ongoing process of evolution produces a by individual methods that it appears impossible at this
spectrum of species that exist in different states of time to systematically favor any one of them (Carstens
separation: from almost identical metapopulations et al. 2013). When different methods return ambiguous
to clearly distinct and isolated lineages. Because delimitations, Miralles and Vences (2013) and Carstens
operational taxonomy typically requires separation et al. (2013) advocate the use of conservative decisions
by one or more of the secondary properties, species (i.e., lumping strategies), as such biases are easier to
within the “gray zone” remain not differentiated in detect and subsequently correct through additional
most cases. studies. This point is worth noting because lumping is
By characterizing operational units through sequence always detrimental to ecological studies (Padial et al.
divergence, molecular taxonomy ventures deeper into 2010).
the “gray zone” than classical taxonomy. The degree The final step in molecular taxonomy is the
to which MOTUs reach into the “gray zone” is a implementation of the resulting MOTUs in a stable
function of the resolution of the molecular marker but flexible nomenclature. Such nomenclature will have
(or markers) used for MOTU delineation. At some to account for multiple levels of genetic variability
level, existing sequence divergence only describes the corresponding to the different stages of acquisition
unique genome of non-clonal individuals and is of no of secondary properties progressively differentiating
taxonomic value. Therefore, the marker(s) on which a a set of metapopulations into distinct morphospecies
molecular nomenclature is based has/have to represent (Fig. 1d). This is best accounted for by a nested
a balance between uniqueness and representativeness nomenclature. Placing MOTUs into a nested structure
(Fig. 1a). For this reason, it is not necessary and provides the advantage of a stable and informative
perhaps even not useful to base species delimitation evolutionary framework, which is more robust for
on whole-genome studies if the level of divergence successive revisions and implementation of new
among molecular taxa can be reduced to the divergence methods and gene markers. Hierarchical nomenclature
a) Uniqueness vs. representativness b) Selection of markers

Specimen
Ind 1 1 1 2 3 4 1 2 3 4 5 6 7 8 9 ...
Ind 2
Population
Ind 3
s
es
Uniqueness
Ind 4
en
iv
Barcode Multi locus Genome wide dataset

us
cl
Cryptic species
In
c) Automated delimitation
Morpho Del 1
species Del 2
Del 3
Del 4

Ind 1
Ind 2
Ind 3
Ind 4
Ind 5
Ind 6
Ind 1
Ind 2
Ind 3
Ind 4
Ind 5
Ind 6
Ind 1
Ind 2
Ind 3
Ind 4
Ind 5
Ind 6
Genome
Multilocus
Agreement Lumping vs Incongruence
Barcode
Conserved Marker splitting
Representativeness
d) Unified molecular nomenclature
Morphospecies A Morphospecies B Morphospecies C
CS-1 CS-2 CS-1 CS-2 CS-1 CS-2
α β γ α β α β α β γ α β γ α β MS-A MS-B MS-C
CS-1 CS-2 CS-1 CS-2 CS-1 CS-2
α β γ α β α β α β γ α β γ α β
MS-A MS-BC
α β γ α α β γ χ δ ε CS-1 CS-2 CS-1
α β γ α α β γ χ δ ε
α β γ α α β α β γ χ δ β
MS-ABC
CS-1 CS-2 CS-3 CS-4 CS-1
α β γ α α β α β γ χ δ β
Common Ancestral Morphospecies

FIGURE 1. Toward a unified molecular nomenclature: Data, constraints, and consequences. a) Relationship between the potential level
of resolution of molecular markers (representativeness), the biological level of uniqueness, and the inclusiveness of the resulting molecular
nomenclature (increasing from morphospecies to specimens). b) Principle of contingency in MOTU delineation based on multiple markers:
when the number of markers used for delineation is increased, the new markers must be linked to the initial set of markers to allow conservation
of MOTU names. c) Three scenarios of changes in MOTU delineation due to new delineation methods and/or new markers (“Del” abbreviation
for delimitation, “Ind” abbreviation for individual). d) An application of the proposed molecular nomenclature on a hypothetical example
of an evolving lineage. MOTU delineation and nomenclature (labeling) is shown at three steps of differentiation under a coalescent process
(tokogeny redrawn and modified after Leliaert et al. 2014). Dots represent metapopulations of a given cryptic species (symbolized by different
color shading) which are differentiating into three morphospecies (solid black contour lines). Ancestor-descendant links are symbolized by lines
between metapopulations. When the nomenclature is applied, each MOTU receives a formal label for each level below the morphospecies level
(in this two-level example, an Arabic number for the cryptic species [CS] level, and a Greek letter for the metapopulation level).
can be implemented with rigid ranks or as a rank-free Units and Typification

system (Benton 2000). A system with ranks is easier to A pragmatic upper boundary for the level of
implement in terms of having a finite number of ranks, inclusiveness of units in the proposed molecular
associated with clear definition and regulated naming. taxonomy is the level of morphospecies, whose
On the other hand, for the same reason as the lack of a nomenclature is de facto regulated by formal
universal barcode, it seems unrealistic to prescribe the morphotaxonomy. Conversely, the lower boundary
number of MOTU ranks. Thus, we propose a semiopen is given by one or several specific DNA substitution
system with a number of ranks (levels), which is fixed patterns observed within a single marker gene
within each taxon of interest but may vary among taxa. (basetype). Where multiple genes are available for
The system is bounded by morphological species on its single individuals, each sequence pattern for each locus
upper level and by unique DNA substitution patterns on is a basetype. It will be essential to strive to identify
the lower level. all gene copies occurring within single individuals
Yeates et al. (2011) proposed to make taxonomy an for each chosen marker (alleles, multiple copies) and
iterative process during which the species boundaries use their diversity to define the lowest MOTU level—
are tested using several lines of evidence and the the basegroup. The basegroup is a set of basetypes,

process is pursued until species boundaries reach where all pairs of basetypes have been observed to
stability. Similarly, Pante et al. (2015) advocated an co-occur within one individual. Two basegroups are
integrative taxonomy loop, where a Primary Species considered as different as long as their basetypes are
Hypothesis is proposed based on morphological or not observed to co-occur within a single individual,
single marker delimitation, and then submitted to an similar to the mutual allelic exclusivity of the haploweb
integrative taxonomy loop involving the addition of of Flot et al. 2010. If only a single gene version exists
new material, alternative species delimitation, or any for every gene marker(s) used for the nomenclature
evidence revealing the presence of a secondary species system, a basegroup will contain only one basetype. The
property sensu de Queiroz (2007). When the addition basegroup is the basis of the nomenclature system we
of new evidence leads to a taxonomic decision, a propose. The hierarchical nature of genetic variability
Secondary Species Hypothesis is proposed and then between the basegroup and the morphospecies level can
subsequently evaluated following the same process, be used to define a number of intermediate nested levels
gradually leading to a more and more stable and to circumscribe units at different levels of divergence.
reliable taxonomy. However, such an iterative process The nature and number of such intermediate levels
can hardly be achieved within a single study, since may differ depending on the clade under scrutiny. We
bringing together the relevant lines of evidence requires stress that every level must be associated with a clear
multiple iterations. In addition, it remains unclear definition, and that objective delimitation methods, or
whether or not such a system would be applicable to clear operational criteria, should be used to circumscribe
cases of incipient speciation (Mittelbach et al. 2007). In the successive levels of genetic variability.
any case, an efficient nomenclature system for MOTUs By defining molecular units in this way,
must be able to accommodate more or less frequent morphospecies may be (or appear) paraphyletic or
revisions. even polyphyletic (Fig. 1d). This situation is likely to be
common and may arise for a variety of reasons (Funk
and Omland 2003). For example, paraphyly may ensue
when one of several (but not all) cryptic species within
DESCRIPTION OF THE PROPOSED ITERATIVE MOLECULAR a morphospecies is associated with a morphological
NOMENCLATURE SYSTEM distinction (i.e., is pseudo-cryptic) and receives its own
A nomenclature system accommodating multiple formal name (Weiner et al. 2015), or it may reflect the
lines of evidence introduced by successive studies using existence of discrepancies between gene phylogenies
single or multiple markers, or even a genome-wide data during the early stages of speciation (Leliaert et al. 2014).
set, and facilitating revisions of the Primary Species Irrespective of its origin, we consider the existence
Hypotheses would provide the required connectivity of nonholophyletic formally named morphospecies
between molecular and morphological taxonomy. It unavoidable and at least provisionally acceptable for
should be flexible enough to allow the incorporation the purpose of formal nomenclature.
of new evidence from automated delimitation methods As in formal nomenclature, stability in the molecular
and the transfer of MOTUs into formal taxonomy on nomenclature system can only be achieved by
the basis of morphometric analyses as well as ecological associating MOTUs with a formal definition based
and biogeographical data. Based on the incorporation of on a type. A MOTU of a higher level would be typified
such new evidence, the molecular nomenclature should by a unique MOTU of a lower level. Therefore, the
allow the transfer of the level and nature of previously definition of each MOTU must include a comprehensive
defined units without compromising the stability of attribution of MOTUs of a lower level, as well as a
names. Upon such transfer, the nomenclature should description of the data and method used to establish
maintain the contingency of all changes and record the the distinctiveness of the molecular clade comprising
reasons motivating such changes. the MOTUs. In case of a revision, the new definition
will have to account for continuity with existing subspecific identifier (like subsp., var., or forma). The
names. The type at the level of a basetype would be latter is to exclude any possibility of confusing MOTU
a unique sequence identified by its accession number names with formal names. Where a MOTU has to be
in a public database and a voucher or a label pointing linked to its diagnosis, its name should be associated
unambiguously to the specimen and clone from which with the publication where it was defined. An example of
the sequence has been obtained. The latter is important a MOTU name would be “Globigerinella siphonifera IIa1”,
when facing intragenomic variability, where there may extended to “G. siphonifera IIa1 sensu Weiner et al. (2014)”
be multiple basetypes found for every chosen marker(s) where necessary. When a hierarchical system is used,
in the same specimen. Also, where multiple markers each MOTU of a lower level must be associated with
have been extracted from the same specimen, it will be exactly one MOTU of a higher level, and each MOTU of
important to establish whether the different markers a higher level must contain at least one MOTU of a lower
have a different level of resolution or reveal conflicting level.
signals (Fig. 1c). Further, next to typification and definition of
The method for delineation of clades is not prescribed, MOTUs, we borrow the principle of priority from
but we note that when a new and promising method formal nomenclature and establish a scheme to avoid

is developed, it should be applied to the taxa under homonymy by transfer or revision. For this, we invoke
scrutiny and associated with a comprehensive revision the concept of MOTU name unavailability in the sense of
to achieve methodological consistency in the molecular the ICZN (1999). When a new MOTU is being defined,
taxonomy. In this context, addition of new data or new its name must be available. Like in formal nomenclature,
genes does not constitute a new method. Ultimately, a delimitation of a MOTU is fixed by first description.
the number of levels between the basegroup and the Unlike formal nomenclature, where the species name is
morphospecies should be tailored to the complexity of fixed, the names of a MOTU will change upon transfer or
the taxonomic group of interest. when their level is revised, even when their delimitation
(diagnosis) remains the same.
The first case where such a situation arises is when a
MOTU is transferred to the morphological species level,
Nomenclature Rules that is, enters formal nomenclature. In this case its name
First, we consider the relationship between MOTUs becomes unavailable, but the names of all other MOTUs
and formal nomenclature. The first guiding principle remain unchanged. The MOTU that is being transferred
is that MOTUs should not enter formal nomenclature, (and its lower-level constituents) will be renamed.
unless they can be diagnosed by some commonly Second, such a situation may arise when the concept of
accepted type of phenotypic trait(s). By diagnosis, we a basegroup is challenged by the observation of several
mean the discovery of a consistent gap in the state of basetypes previously assigned to different basegroups
one or more phenotypic characters between the MOTU within the same individual. In this case, the new
of interest and all its siblings. The definition of the gap basegroup will contain all the basetypes of the former
(or discontinuity) should follow the criteria typically basegroups plus the new ones, leading to a new name.
used for morphological taxonomy of the studied The names of the basegroups lumped into the new, more
group. Ecophenotypy is pervasive among animal and inclusive basegroup all become unavailable.
plant taxa. Therefore, we recommend that when a Third, when the definition of a MOTU changes such
MOTU is diagnosed as a morphospecies, it should that some of its constituent MOTUs are removed or
first be demonstrated that the diagnosis is applicable others are added, the newly defined MOTU will obtain
throughout the range and habitats of the newly named a new denomination and its former name will become
morphospecies. unavailable.
In many cases, post-hoc assessments of cryptic genetic Fourth, we recommend defining a convention for the
diversity yielded evidence for the existence of diagnostic naming of the MOTUs using a succession of fields using
phenotypic traits (Hebert et al. 2003), so the molecular different case types for each successive level of the
nomenclature system must be able to accommodate nomenclature (e.g., Roman or Arabic numerals, lower
a transfer of a MOTU into the formal nomenclature. or upper case roman, or Greek letters). For instance,
Because of the often decoupled rates of molecular and in the case of a three-level nomenclature system, we
phenetic divergence and the very nature of incipient propose to use a combination of upper case Roman
speciation, the transfer would often be limited to a numerals, followed by one or more lower case letters,
subset of MOTUs of a lower level within a MOTU and an Arabic numeral: Genus species IIa1. When one
of a higher level. In such situations, rules are needed category of symbol is exhausted due to a large number
to prevent renaming of MOTUs removed from (or of categories or successive renaming, we recommend
left abandoned in) a morphological species and to doubling it: Genus species IIaa1. In this way, increasingly
ensure that denominations of MOTUs shifted to a complex combinations can be easily elaborated in the run
morphological species will never be used again. of successive revisions unveiling a deeper hierarchical
We propose that the name of each MOTU consists structure requiring additional nested levels (e.g., Ia1 →
of the name of its parent morphospecies and a AIa1 → AIa1 → …). The finest level is always at the
hierarchically structured denomination, without any right end of the name.
Finally as progress in sequencing technologies reduce objective analysis of sequence diversity. Göker et al.
analytical costs, more marker genes will become (2010) explored a clustering optimization approach,
available, especially for groups where the genome while André et al. (2014) used two complementary
is currently unknown. Therefore, additional marker approaches for automated delineation of genetic
gene(s) can be included in the nomenclature when clusters, namely GMYC (Pons et al. 2006) and ABGD
available, and will constitute additional basetype(s) (Puillandre et al. 2012b). In both cases, the authors
keeping consistency with the available marker (Fig. 1b). concluded that a unique threshold related to a consistent
The rules above only apply to the definition of MOTUs. level of genetic divergence could not be found to
Attribution of unknown sequences, in contrast, can be circumscribe taxa within the group as a whole. In
made to any level in the nomenclature hierarchy of analogy with what is observed in other taxonomic
MOTUs. Any observation yielding sufficient genetic groups (Carstens et al. 2013), ABGD- and GMYC-based
information unambiguously assignable to a given delineations of planktonic foraminifera species are rarely
MOTU level can be used to investigate the ecology, congruent, leading the authors to favor conservative
biogeography, or evolution of this given MOTU. This (i.e., lumping) solutions to avoid over-interpretation
applies to sequences only partially covering the chosen of the results (André et al. 2014). These incongruent

gene region, environmental sequences lacking by nature results between ABGD and GMYC are due to an
an attribution to a given specimen, or a RFLP pattern extreme heterogeneity of substitution rates and complex
accounting for the presence of a diagnostic sequence evolutionary patterns of the SSU rDNA in planktonic
pattern in a given specimen. foraminifera. For instance, an extensive survey of the
morphologically diverse Trilobatus sacculifer did not
show any sign of cryptic diversity (Fig. 3; André et al.
2013), whereas a comparable sampling and sequencing
THE CASE OF PLANKTONIC FORAMINIFERA effort identified G. siphonifera as a hyperdiverse species
As in many other taxa (Bickford et al. 2007) and complex (Weiner et al. 2014, 2015). Sharing almost
most particularly among protists (Kosakyan et al. 2013), identical morphology, the three distinct lineages of
morphospecies in planktonic foraminifera were shown Orbulina universa seem to have diverged millions of
to harbor considerable cryptic diversity (de Vargas years ago (de Vargas et al. 1999; Morard et al.
et al. 1999; Darling and Wade 2008), some of the 2009), whereas “genotypes” of Globigerinoides elongatus
detected genetic entities being associated with subtle represent shallow divergences (Aurahs et al. 2011), if not
but significant morphological differences (Darling et al. a population signal (André et al. 2014).
2006; Morard et al. 2009, 2011; Aurahs et al. 2011; Until now, there has been no evidence found for
Quillévéré et al. 2013; Weiner et al. 2015). Nevertheless, hybridization among any of the described MOTUs
the majority of the discovered genetic diversity has not in planktonic foraminifera. Although these lines of
been linked so far to any morphological differences and evidence alone are not sufficient to unambiguously
most MOTUs (cryptic species) of planktonic foraminifera equate the observed genetic diversity with reproductive
remain formally nameless (André et al. 2014). isolation, they collectively speak for the existence of
The last decade has seen an increase in genotyping reproductively isolated cryptic species in planktonic
studies in planktonic foraminifera carried out by foraminifera. Protists are rarely amenable to breeding
different research teams. This resulted in the existence experiments, which ultimately prevents direct
of multiple, often inconsistent molecular nomenclatures, confirmation of the level of genetic divergence
as is the case, for example, for the successive studies of corresponding to the biological species (but see Amato
the genus Globigerinella (Fig. 2). In addition, the lack of et al. 2007). Therefore, the only levels of divergence
clarity concerning the level of genetic and morphological in planktonic foraminifera that can be identified
divergence that represents biological species would unambiguously with current methods are represented
likely lead to frequent, large-scale taxonomic revisions. by the collocated sets of mutations characterizing a
For this reason, the genetically circumscribed entities, unique ribosomal sequence (motif), the set of motifs
variously referred to as “clades”, “genetic types”, present within an individual, and the level of genetic
“genotypes”, “subtypes”, “phylotypes”, “ribotypes”, divergence that is manifested morphologically and can
“ecotypes”, “haplotypes”, “sequence motifs”, “cryptic be treated by formal taxonomy. Because it is not possible
species”, or “genetic species”, received informal labels to directly test for interbreeding, we cannot determine
(e.g., Huber et al. 1997; de Vargas et al. 1999) typically which of the levels of the hierarchical structure
reflecting the hierarchical phylogenetic structure of the in the genetic diversity of planktonic foraminifera
classified units (Darling et al. 2003). Initially, such labels corresponds to biological species (see also Leavitt et al.
have been given without an explicit assignment of a type 2015). A solution to this problem may be found at
sequence (typification). Their definitions made use of some stage in the future, but for now, we consider it
different marker genes, and due to large heterogeneity an additional advantage of a hierarchical taxonomy
in substitution rates (de Vargas et al. 1997), they were not that it leaves open where the exact level of biological
based on universal thresholds. species occurs in each clade. It is very likely that within
To date, two attempts have been made to delineate a given morphospecies, the level of biological species
MOTUs in planktonic foraminifera as a whole by an will correspond to the same level in the hierarchy.
I II Huber et al. (1997)

a)
I IIa IIb Darling et al. (1999)
I II III IV de Vargas et al. (2002)
Ia1 Ia2 IIa IIb cal Darling and Wade (2008)
I II III IV Ujiié and Lipps (2009)
I II III André et al. (2014)
Ia Ib IIa1 IIa2 IIa3 IIa4 IIa5 IIa6 IIb IIIa IIIb IIIc Weiner et al. (2014)
Globigerinella Globigerinella Weiner et al. (2015)
Globigerinella siphonifera
radians calida
Abundance

90°N
0.2
b)
60°N
0.15
30°N
Eq 0.1
30°S
0.05
60°S
90°S 0
1 8 0° W 120°W 60°W 0° 60°E 120°E 180°E
FIGURE 2. History of the molecular nomenclature of the three morphospecies within the planktonic foraminifera genus Globigerinella. a)
Continuity of names of the different MOTUs among the successive studies listed chronologically, from the initial work of Huber et al. (1997)
up to the last taxonomic revision by Weiner et al. (2015). Each rectangle represents the MOTUs described in each successive study and their
connectivity is given by the strips; rectangles with a gray background highlight the renaming of a MOTU between two studies. b) Geographic
origin of the sequences produced in the successive studies (same labels as in a). Background shading shows the relative abundance of the genus
Globigerinella in surface sediments as an index of the morphospecies distribution (from Weiner et al. 2014).
IMPLEMENTATION IN PLANKTONIC FORAMINIFERA the sequence, as defined in Morard et al. (2015), should
Based on the general principles presented above, optimally have been observed several times (we suggest
we exemplify hereafter the criteria that allow us to here using three times as a minimum threshold) in
implement such a nomenclature scheme in the case of the available data set, either by technical or biological
planktonic foraminifera. We stress that the criteria given replicates, to validate the observed sequence pattern as
in this work are a starting point based on currently a genuine biological signal. In the case of intragenomic
available evidence and methodologies; these criteria variability, the sequencing effort must be scaled to the
may obviously evolve in the future. amount of diversity within the target morphospecies.
In summary, each unique sequence pattern observed
multiple times and at least once in a sequence covering
Basetype Definition in Planktonic Foraminifera the entire marker is considered a basetype.
We propose to define basetypes in planktonic
foraminifera (Fig. 4) by using sequence patterns in the
rDNA fragment located at the 3 -end of the SSU rRNA Nomenclature System
gene, between stems 32 and 50 (Wuyts et al. 2001). The proposed planktonic foraminifera molecular
This fragment has been proposed as the barcode for nomenclature system is organized in a three-level
benthic foraminifera (Pawlowski and Holzmann 2014). system (Fig. 4c) deemed to be intraspecific with respect
It captures enough phylogenetic signal (Darling and to the formal nomenclature regulated by the ICZN
Wade 2008) and harbors six variable regions, three of (1999). The nomenclature is built only on basetypes
them being specific to foraminifera (Pawlowski and validated by multiple observations. In principle, for the
Lecroq 2010). The sequence pattern of each region of reasons outlined above, any of the three levels could be
Globigerinoides ruber pink

0.1 Globigerinoides ruber Ia
Globigerinoides ruber Ib
Globigerinoides ruber IIb
Globigerinoides elongatus IIa1
Globigerinoides elongatus IIa2
Globigerinoides conglobatus
Orbulina universa I
Orbulina universa II
Orbulina universa III

Trilobatus sacculifer
Trilobatus trilobus
Trilobatus immaturus
Trilobatus quadrilobatus
Globigerinella radians Ib
Globigerinella siphonifera Ia
Globigerinella siphonifera IIb
Globigerinella siphonifera IIa2
Globigerinella calida IIIc
Globigerinella calida IIIa
Globigerinella calida IIIb
FIGURE 3. Decoupling of rates of molecular and morphological evolution in planktonic foraminifera. This molecular phylogeny shows the
relationships between 11 morphospecies (illustrated by sketches of representative specimens) belonging to the genera Globigerinoides (Aurahs
et al. 2011), Orbulina (de Vargas et al. 1999; Morard et al. 2009), Trilobatus (André et al. 2013; Spezzaferri et al. 2015) and Globigerinella (Weiner et al.
2014, 2015), based on their SSU rDNA sequence motifs. The solid, dashed, and dotted lines drawn on the tree show the position of morphological
species, and higher and lower levels of genetic divergence as used in the cited studies, respectively. The vertical bars to the right of the taxon
names highlight the incongruence between resulting molecular and morphological taxonomies.
considered a Primary Species Hypothesis sensu Pante represents the intragenomic (individual) variability,
et al. (2014) and represent a working hypothesis. whereas the variability observed among different
basegroups is considered to represent at least the level
MOTU level 3.—The lowest level corresponds to of population variability (Fig. 4).
the basegroup and represents the genetic variability
potentially observable at the level of a single individual. MOTU level 2.—The intermediate level most likely
Thus, by definition different basegroups contain represents the level of biological species. It is defined
basetypes that are never observed together. In the case as a monophyletic cluster of one or several basegroups,
of the absence of intragenomic variability, such as in delineated by an objective method searching for the
many spinose planktonic foraminifera, the basegroup most likely level of divergence reflecting reproductive
may contain only one basetype. The basegroup is isolation. André et al. (2014) showed that ABGD
the basic unit of the nomenclature system proposed (Puillandre et al. 2012b) or GMYC (Pons et al. 2006) can
here; it is the only level grounded on empirical data. be used to objectively delineate MOTUs in planktonic
The variability observed within a given basegroup foraminifera. In the case of conflicting delineations and
Accession a) Basetype definition b) Basegroup constitution

number 32-37 37F 37-41 41F 39-43 43E 44-45 45E-47F 47-49 49E 50
ZZ0001
7 7 9 5 6
ZZ0012 Basetype
ZZ0134
3 7 9 5 6
ZZ0185 Basetype
Basetype
ZZ1102
ZZ2163
3 7 9 3 6
ZZ4158 Basetype
ZZ1278
ZZ7843
3 3 9 5 6
ZZ9815 Basetype
3 3 9 5 1 a b c d e f g h i j k
ZZ4176 Specimen
ZZ1587
c) Nomenclature scheme
C1) Definition of MOTUs

Genus species-a Morphospecies
I II MOTU level - 1
a b c d a b MOTU level - 2
1 1 1 1 1 2 1 MOTU level - 3
C2) MOTU IIa diagnosed by phenotypic features

Genus
Genus species-a species-b
I II I
a b c d a b a
1 1 1 1 1 1 2
C3) Description of new basegroups and transfer of basegroups to MOTUs

Genus
Genus species-a species-b
I II I
a b c d a b c d a b c
1 2 1 1 1 1 1 1 1 1
C4) Taxonomic revision: lumping of MOTUs. Genus species-a II transfered

to Genus species-c I. Names in white rectangles become unavailable.
Genus Genus
Genus species-a species-b species-c
III I I
abc d e a b c d a b c d a b c
1 2 1 1 2 1 2 1 1 1
FIGURE 4. A guide for the definition of MOTUs in planktonic foraminifera. a) The selected gene for planktonic foraminifera is the fragment
located at the 3 -end of the SSU rDNA, between stems 32 and 50 (Wuyts et al. 2001). The sequences are partitioned in their constitutive variable
(lines) and conserved (rectangles) regions, following Morard et al. 2015. In this example, the different line colors represent unique sequence
motifs found in the available data set; the position of each region is given above the first sequence. Only sequences covering the entire fragment
and sequences for which each individual region has been observed at least three times in the available data set (number of observations given
above the lines) are designated as basetypes. In this example, five sequences have the required length and four can be designated as basetypes
(ZZ1587 is long enough but has a sequence motif for the region 49E which is observed only once in the data set). b) Occurrences of basetypes
(rows) within a set of individuals (columns). The different symbols represent the different basetypes occurring within (when situated on the
same column) and between (when situated on the same row) individuals. A basegroup is defined as a network of basetypes connected by
pairwise co-occurrence, represented by solid lines. In this way, two basetypes can be grouped in the same basegroup even if they were not
observed co-occurring in the same specimen. When intra-individual variability is discovered, we recommend generating at least 10 full-length
clones for a few selected specimens in order to cover the intragenomic variability occurring within a given MOTU. c) The nomenclature scheme
allows the transfer of MOTUs to higher levels, splitting and lumping of existing MOTUs, and the inclusion of new basegroups, as illustrated
in a succession of theoretical nomenclature acts ((c1)–(c4)). The intra-morphospecies nomenclature we propose for planktonic foraminifera is
based on a three-level hierarchical system (e.g., “Ia1”, meaning: MOTU level-1 “I” includes MOTU level-2 “a” includes MOTU level-3 “1”) (Case
(c1)). The nomenclature is amended as soon as the status of the previously defined MOTUs is modified based on morphological, molecular, or
ecological evidences. In the case of transfer to a higher-level taxon (Case (c2)), splitting one MOTU into two distinct ones (Case (c3)), or lumping
of two MOTUs into a single one (Case (c4)), names of amended MOTUs become unavailable (dotted gray rectangles). In the case of a revision
with “steps backward” (as for the MOTUs Genus species-b Ia1 and Genus species-b Ia2 in (c2), which are split into Ib1 and Ic1 in (c3) and merged
again in (c4)), a new MOTU name is used. In the case of objective synonymy, we follow the same principle of priority as for the ICZN (1999).
for nomenclature purposes, we recommend the use of very different substitution rates for the same marker
the most conservative boundary for species delineation gene.
in planktonic foraminifera—that is, lumping rather than
splitting, following Carstens et al. (2013) and Miralles
and Vences (2013). Because automated delineation is a
dynamic research field, new methods may arise in the FURTHER CONSIDERATIONS
future, making the status (or level) of the second level The proposed MOTU nomenclature may be applied
MOTU likely to be reevaluated. In addition, sequences to any other taxa which display a hierarchically
from new markers may be used to assess the validity of structured genetic diversity occurring below the level
the second level MOTU based on the current SSU rRNA of morphospecies. MOTU implementation for a given
marker. group could serve as a framework to associate metadata
to a consistent level of genetic divergence. Consistent
application of the proposed molecular taxonomy to
MOTU level 1.—Represents the highest intra- sequences from individuals as well as environmental
morphospecific level designed in the proposed sequences will allow a reproducible and reliable

nomenclature scheme; it is defined as a monophyletic association of MOTUs with ecological data, geographic
cluster of intermediate-level MOTUs (i.e., putative origin, time and depth of collection, behavior, associated
biological species) reflecting a major disruption microbiome, or morphology. The criteria of such
in the genetic variability observed within a given nomenclature (genetic threshold between two identical
morphospecies. This level is considered to represent levels of the same MOTUs) could in theory be
ancient and well-established divergences within propagated into environmental data sets with novel
the morphospecies evolutionary history; it is likely sequence motifs not linked to organisms, even in such
to represent at least the level of biological species. situations where no unique threshold can be applied
Optimally, this level should be statistically significantly to the entire group. The use of a MOTU-specific
supported as monophyletic and it should always be threshold as a working hypothesis will lead to a more
delineated objectively. For example, its status can be accurate interpretation of the metagenomic data. In
established by using a barcode gap delineation method this respect, the proposed molecular taxonomy scheme
such as ABGD, using the coarsest partitioning given by will serve both as a tool to preserve existing work
the method within a morphospecies. and to hierarchically explore new and increasingly
We exemplify this nomenclature scheme through complex data sets. In addition, in the case of a revision
two cases: the Globigerinella species complex, which of the taxonomy, metadata linked to MOTUs can be
is characterized by a large genetic diversity and a automatically transferred into the revised categories.
disconnection between morphological and molecular On the other hand, the proposed nomenclature system
evolution (Weiner et al. 2015; Fig. 5), and the shows some weaknesses that should not be ignored.
morphospecies Pulleniatina obliquiloculata, which is First, it is not primarily meant to name unknown
characterized by a large intragenomic variability (Ujiié clades from environmental sequences. Because it is
et al. 2012; Fig. 6). The methodology used to delineate tied to formal nomenclature, the morphotaxonomical
the MOTUs is detailed in the figure captions. The identity of the specimen from which the sequences
Globigerinella species complex is composed of 10 MOTUs are derived must be first established or the molecular
(MOTU level 3) structured into five putative species taxonomy becomes detached from formal taxonomy. In
(MOTU level 2) constituting three genetic lineages the proposed scheme, it is not possible to create artificial
(MOTU level 1). Attribution of these MOTUs to categories based solely on molecular characters in order
morphological species results in paraphyly as there to classify sequences of unknown origin. Second, the
is a clear disconnection between morphological and system works best when the magnitude and structure
molecular evolution within this species complex. of the diversity within the group are known. Otherwise,
Pulleniatina obliquiloculata is composed of 36 MOTUs the result of the iterative process of testing species
(MOTU level 3) structured into two putative species hypotheses will be a nomenclature with many “holes”.
(MOTU level 2) and a single genetic lineage (MOTU This is unfortunate, but unavoidable, and we thus
level 1). advocate for an application of the taxonomic scheme not
These examples show that a consistent application before a sufficient amount of data covering a significant
of the proposed system will be largely congruent with part of the ecological and biogeographical ranges of the
original studies, but will likely change the levels of the studied taxa is already available. Clearly, the existence
MOTUs. Since MOTUs have been described initially of a comprehensive database covering the taxonomic,
from partial sequences, the new scheme will decrease biogeographic, and ecological range of the group of
the number of MOTUs of intermediate level, unless a interest such as the one developed by the authors of this
systematic sequencing effort is carried out to provide article (Morard et al. 2015) is a strong prerequisite for
full-length sequences (basetypes) for all observed motifs. the establishment of a molecular nomenclature. Third,
The application also highlights the advantage of the while the scheme remains reasonably flexible, we note
system of not being linked to a single threshold, that frequent revisions will inevitably complicate the
thus allowing consistent classification of MOTUs with nomenclature, especially by generating lengthy lists
a) Basetype definition N observation b) Basegroup constitution

300
89 sequences
validated
100
Specimen
BRBR14SIPI
CAG.sII2A
CAG.sII6B
LPBANF
PO117
PO144
PO146
PO154
PO170
PO180
PO186
PO201
PO240
PO248
PO252
CA06B
CA02a
AS195
AS273
CB01a
PO13
PO16
PO20
PO22
PO24
PO26
A493
A526
P11b
2163
2168
3004
6606
8449
BR14
BR18
P125
OKI2
OKI3
OKI5
P11
P27
LPB
KM194180
KF769861
KF769820
Z83959
KF769822
10 KF769629
385 sequences not validated
JQ799892
SEQUENCES
KM194179
KM194223
KF769582
AB263453
BASETYPE
AB263455
PO266
PO270
PO271
PO274
PO279
PO283
PO284
PO291
PO295
PO304
PO318
PO337
PO346
PO347
PO28
PO31
PO33
PO37
PO38
PO42
PO43
PO50
PO51
PO62
PO63
PO65
PO67
PO68
PO70
PO80
PO81
PO83
PO85
PO88
PO97
PR18
R043
NA-1
NA-2
NA-3
SB05
SB10
SB22
KM194180

KF769861
KF769820
Z83959
KF769822
KF769629
1 JQ799892
KM194179
KM194223
KF769582
AB263453
AB263455
0
12 unique basetypes
F
10 basegroups
-4
-4
-4
-4
37
41
47
43
49
1 3 6 9 86 specimens
37
39
44
47
E-
N validated
45
Region region
c) Molecular nomenclature
G. radians G. siphonifera G. calida
I II I
10% a a b c a
3 morphospecies
Globigerinella Globigerinella 3 genetic lineages (MOTU level-1)

Globigerinella siphonifera Morphospecies
radians calida
I II I MOTU Level - 1 5 putative species (MOTU level-2)
a a b c a MOTU Level - 2
10 MOTUs (MOTU level-3)
MOTU Level - 3
1 2 2 1 2 1 2 2 1 2 3 1
FIGURE 5. Implementation of the molecular nomenclature system for the genus Globigerinella. a) The heatmap represents the 474 sequences
belonging to Globigerinella available in the PFR2 database v.1 (Morard et al. 2015). Each column represents an individual variable region of the SSU
rDNA gene; colors represent the number of observations of a given sequence motif. For each region, only sequence patterns (motifs) observed at
least three times are validated and only the sequences for which nine regions are validated are retained for the molecular nomenclature, leading
to 89 sequences validated. b) Among the 89 retained sequences, 12 unique sequence patterns are retained as basetypes. Basetypes co-occurring
within the same individual(s) (marked by stars, two cases) are grouped within the same basegroup. c) The 12 basetypes were automatically
aligned with MAFFT v. 7 (Katoh and Standley 2013) and a phylogenetic reconstruction was performed with PhyML (Guindon et al. 2010) under
the model (GTR+I) chosen with jModeltest v. 2.1.7 (Darriba et al. 2012). The same alignment was subjected to Automatic Barcode Gap Delimitation
(ABGD, Puillandre et al. 2012b), using the default setting of the program and the K-80 distance to classify the basetypes into putative species.
The first MOTU plateau was retained as putative species (MOTU level 2), and the lowest plateau was retained to identify the major disruption
of genetic variability of the species complex (MOTU level 1). The three morphotypes occurring within Globigerinella identified by Weiner et al.
(2015) were implemented in the taxonomy as an upper boundary. All data necessary to produce the nomenclature and resulting files are available
in Supplementary Material S1, available on Dryad at http://dx.doi.org/10.5061/dryad.64pg3.
of unavailable names. Therefore, we recommend that to make the nomenclature tractable and thus useful.
a revision of the nomenclature should be attempted Ultimately, it remains left to the taxonomist to evaluate
only when a significant new input is provided. Indeed, the balance between stability and reliability. Last, the
nothing excludes a revision when only a limited number nomenclature system described here is currently not
of sequences for a given taxa are available, but a certain formally codified, making its application grounded
degree of stability is necessary between each revision on a voluntary basis. Therefore, it will require a
a) Basetype definition N observation

b) Basegroup constitution
300
52 sequences
Specimen
validated
GYA1037
GYA1508
GYA1828
GYA2395
GYB1810
GYA280
GYA478
GYA549
GYB650
KH1431
KH1623
Me1594
Ama10
Ama13
Ama17
Ama21
Ama26
Ama27
KH279
KH343
Y1211
Y1220
Y1224
Y1441
Y1442
Y1446
Y1448
Y1484
Y1492
Z232
Z329
Z330
Z362
Z511
OKI1
OKI2
100
NA
AB636743
AB636744
AB636745
AB636924
AB636737
AB636740
AB636914
AB636704
AB636705
AB636824
AB636703
10 AB636806
AB636807
SEQUENCES
AB636728
AB636726
219 sequences not validated
AB636727
AB636689
AB636720
BASETYPE
AB636734
AB636908
AB636889
AB636901
AB636701
2 AB468840
AB468841
AB636694
AB636712

AB636713
AB636842
AB636714
AB636841
AB636695
AB636783
AB636784
AB636724
1 AB636722
AB636716
AB636698
AB636791
AB636683
AB636756
AB636685
AB636686
AB636765
AB636766
AB636687
0 DQ407271
F
E
-4
-4
-4
-4
37
41
47
43
49
1 3 6 9 47 unique basetypes
37
39
44
47
E-
N validated 36 Basegroups
45
Region region
37 specimens
c) Molecular nomenclature
Pulleniatina obliquiloculata 1 morphospecies
10%
I 1 genetic lineage (MOTU level-1)
a b 2 putative species (MOTU level-2)
36 MOTUs (MOTU level-3)
Morphospecies
Pulleniatina obliquiloculata
MOTU Level - 1
I
MOTU Level - 2
a b
MOTU Level - 3
1 1 2 3 4 4 5 1 6 6 7 8 4 9 10 8 1 2 3 4 5 6 4 4 7 8 9 8 10 11 12 13 1426 15 16 17 18 19 20 21 22 23 24 25 25 8
FIGURE 6. Implementation of the molecular nomenclature system for the morphospecies Pulleniatina obliquiloculata. a) The heatmap represents
the 271 sequences belonging to P. obliquiloculata available in the PFR2 database v.1 (Morard et al. 2015). Each column represents an individual
region of the rDNA gene; colors represent the number of observations of a given sequence motif. For each region, only sequence patterns
(motifs) observed at least three times are validated and only the sequences for which nine regions are validated are retained for the molecular
nomenclature, leading to 52 sequences validated. b) Among the 52 retained sequences, 47 unique sequence patterns are retained as basetypes.
Basetypes co-occurring within the same individual(s) (marked by stars, seven cases) are grouped within the same basegroup. c) The 47 basetypes
were automatically aligned with MAFFT v. 7 (Katoh and Standley 2013) and a phylogenetic reconstruction was performed with PhyML (Guindon
et al. 2010) under the model (GTR+I+) chosen with jModeltest v. 2.1.7 (Darriba et al. 2012). The same alignment was subjected to Automatic
Barcode Gap Delimitation (ABGD; Puillandre et al. 2012b), using the default setting of the program and the K-80 distance to classify the basetypes
into putative species. The first MOTU plateau was rejected as it sorted basetypes of the same basegroup into different groups. The second MOTU
plateau was retained as putative species (MOTU level 2), and the lowest plateau was retained to identify the major disruption of genetic variability
of the morphospecies (MOTU level 1). All data necessary to produce the nomenclature and resulting files are available in Supplementary Material
S2, available on Dryad at http://dx.doi.org/10.5061/dryad.64pg3.
certain degree of communication and collaboration evolvability; it can be established with modest Sanger
within the community generating the nomenclature sequencing effort and expand to genome-scale data sets
to promote its reliability, efficiency, and therefore its in a straightforward way, therefore including any lines
usefulness. Despite these limitations, we feel that, on a of evidence or concepts to name MOTUs in any domain
community agreement basis, our approach offers a good of the living realm for present and future molecular data
compromise between stability, reliability, flexibility, and sets.
CONCLUSIONS System”. This study is a contribution to the effort of the

The nomenclatural system we propose here does not SCOR/IGBP Working Group 138 “Modern planktonic
replace but complements the currently valid codes for Foraminifera and ocean changes”.
biological nomenclature (ICZN 1999; ICN 2011; ICTV
2011; Garrity et al. 2015). In other words, it is tied to
ACKNOWLEDGMENTS
formal nomenclature as regulated by current codes at
the morphospecies level, but does not overlap with The authors are thankful to Bryan Carstens and four
them, so that no conflict can result from the use of this anonymous reviewers, as well as to Adrian Paterson
nomenclatural system with respect to any one of these (Associate Editor) and Frank Anderson (Editor in chief)
formal codes. For planktonic foraminifera, its success who provided constructive and encouraging comments
and usefulness rely on the community observing the that helped us to improve the present manuscript.
rules, albeit on a voluntary basis. For example, the
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Syst. Biol.

Nomenclature for the Nameless: A Proposal for an Integrative Molecular Taxonomy of

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biogeography, ecology, and conservation biology. Over

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a) Uniqueness vs. representativness b) Selection of markers

Barcode Multi locus Genome wide dataset

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Common Ancestral Morphospecies

can be implemented with rigid ranks or as a rank-free Units and Typiﬁcation

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I II Huber et al. (1997)

I II III IV de Vargas et al. (2002)

Ia1 Ia2 IIa IIb cal Darling and Wade (2008)

I II III IV Ujiié and Lipps (2009)

I II III André et al. (2014)

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Globigerinoides ruber pink

Globigerinoides ruber IIb

Globigerinoides elongatus IIa1

Globigerinoides elongatus IIa2

Orbulina universa III

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Globigerinella siphonifera IIb

Globigerinella siphonifera IIa2

Globigerinella siphonifera IIa4

Globigerinella siphonifera IIa4

Globigerinella siphonifera IIa1

Globigerinella siphonifera IIa5

Globigerinella siphonifera IIa6

Globigerinella calida IIIc

Globigerinella calida IIIa

Globigerinella calida IIIb

Accession a) Basetype definition b) Basegroup constitution

C1) Definition of MOTUs

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C2) MOTU IIa diagnosed by phenotypic features

C3) Description of new basegroups and transfer of basegroups to MOTUs

C4) Taxonomic revision: lumping of MOTUs. Genus species-a II transfered

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a) Basetype definition N observation b) Basegroup constitution

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Globigerinella Globigerinella 3 genetic lineages (MOTU level-1)

a) Basetype definition N observation

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CONCLUSIONS System”. This study is a contribution to the effort of the

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