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Received: 28 July 2017 | Revised: 12 December 2017 | Accepted: 13 December 2017

DOI: 10.1111/mec.14486

INVITED REVIEWS AND SYNTHESES

Cryptic species as a window into the paradigm shift of the

species concept

Cene Fi
ser1 | Christopher T. Robinson2,3 | Florian Malard4

1
SubBio Lab, Department of Biology,
Biotechnical Faculty, University of Ljubljana, Abstract
Ljubljana, Slovenia The species concept is the cornerstone of biodiversity science, and any paradigm shift in
2
Department of Aquatic Ecology, Eawag,
the delimitation of species affects many research fields. Many biologists now are embracing
D€
ubendorf, Switzerland
3
Institute of Integrative Biology, ETH a new “species” paradigm as separately evolving populations using different delimitation
Z€urich, Z€
urich, Switzerland criteria. Individual criteria can emerge during different periods of speciation; some may
4
 Lyon, Universite
Universite  Claude Bernard never evolve. As such, a paradigm shift in the species concept relates to this inherent
Lyon 1, CNRS, ENTPE, UMR5023 LEHNA,
Villeurbanne, France heterogeneity in the speciation process and species category—which is fundamentally
overlooked in biodiversity research. Cryptic species fall within this paradigm shift: they are
Correspondence
Cene Fi
ser, SubBio Lab, Department of continuously being reported from diverse animal phyla but are poorly considered in current
Biology, Biotechnical Faculty, University of tests of ecological and evolutionary theory. The aim of this review is to integrate cryptic
Ljubljana, Ljubljana, Slovenia.
Email: cene.fiser@bf.uni-lj.si
species in biodiversity science. In the first section, we address that the absence of morpho-
logical diversification is an evolutionary phenomenon, a “process” counterpart to the long-
Funding information
PHC Proteus programme, Grant/Award
studied mechanisms of morphological diversification. In the next section regarding taxon-
Number: 31199UM; the Slovenian Research omy, we show that molecular delimitation of cryptic species is heavily biased towards dis-
Agency, Grant/Award Number: P0-0184; the
tance-based methods. We also stress the importance of formally naming of cryptic species
Swiss National Science Foundation, Grant/
Award Number: IZK0Z3_169642; COST for better integration into research fields that use species as units of analysis. Finally, we
Action DNAqua-Net, Grant/Award Number:
show that incorporating cryptic species leads to novel insights regarding biodiversity pat-
CA15219; COST (European Cooperation in
Science and Technology) programme terns and processes, including large-scale biodiversity assessments, geographic variation in
species distribution and species coexistence. It is time for incorporating multicriteria spe-
cies approaches aiming to understand speciation across space and taxa, thus allowing inte-
gration into biodiversity conservation while accommodating for species uncertainty.

KEYWORDS
Amphipoda, biodiversity patterns, convergent evolution, integrative taxonomy, phylogenetic
niche conservatism, speciation

Glossary: Brownian motion, A model of trait evolution, sometimes called random walk, which assumes neutral and gradual evolution of traits due to genetic drift. Change in mean phenotype
is expected to be nondirectional and occurs at a constant rate, whereas variance among species is linearly related to the amount of time since divergence.; Eltonian ecological niche, A
concept of ecological niche defined by the place a species takes in its biotic environment that is, “its relationship towards food and enemies” and the functional role it plays in the ecosystem.;
Grinellian ecological niche, A concept of ecological niche grounded on species requirements for a specific habitat a niche is parametrized with conditions in which a species persists and
breeds.; Integrative taxonomy, An interdisciplinary approach in delimiting species, based on confrontation of genetic, morphological, behavioural and ecological evidence of lineage separation.;
Monophyletic group, A group of organisms composed of a common ancestor and all its descendant species.; Morphological crypsis, Extreme similarity of morphological phenotypes of two or
more species. In this review, we use this term for those species whose morphological differentiation cannot be told apart without prior molecular analysis.; Orstein-Uhlenbeck model, A model
of trait evolution, sometimes also called a “rubber band”, which is an alternative model describing the response of a phenotype to stabilizing selection. Evolutionary changes are constrained
by a constant force towards an adaptive optimum.; Paraphyletic group, A group of organisms derived from a common ancestor, which excludes some descendants.; Polyphyletic group, A
group of organisms derived from different ancestors.; Species concept vs. species taxon, Several authors argued that much of the confusion related to the term species is of semantic nature.
The “species concept” treats species as evolutionary entities. “Species taxon” has practical value. It is an elementary unit in biodiversity research, and individuated by delimitation methods.
The correspondence between species concept and species taxon is unclear and depends on the context of speciation. For this reason, the “species taxon” is a hypothesis of the evolutionary
entities emerging through the process of speciation; White noise model, A model of trait evolution representing a process in which variation of phenotypic traits revolves constantly around
moving trait optima, which generates evolutionary phenotypic change that is independent from phylogenetic relationships.

Molecular Ecology. 2018;27:613–635. wileyonlinelibrary.com/journal/mec © 2018 John Wiley & Sons Ltd | 613

614 | FISER
1 | INTRODUCTION
Genes, species and ecosystems are three major components of bio-
diversity. Among them, species has proven the most challenging to
conceptualize. Decade-lasting disputes over the species concept
yielded no less than 24 species definitions (Mayden, 1997). Defining
a species is central to biodiversity science (Mayden, 1997; de
Queiroz, 1998, 2005b) because any change in the species concept
directly affects many important research fields, including taxonomy,
biogeography, ecology, conservation and macroevolution (Agapow
et al., 2004).
An important step forward was made with a distinction between
conceptual and operational issues, what a species is and how they
should be delimited (Bock, 2004; Hey, Waples, Arnold, Butlin, & Har-
rison, 2003). Most authors today agree conceptually (species con-
cept, see Glossary), that species are entities emerging from the
speciation process as separately evolving segments of metapopula-
tion lineages (Bock, 2004; Hey, 2006; Hey et al., 2003; Mayden,
1997; de Queiroz, 1998). Establishing the correspondence between
the species concept and species taxa, that is elementary units used
in biodiversity research (see Glossary), remains a challenge. From a
temporal point of view, a species is framed by a speciation event, at
the origin of this process, and by event putting an end to this spe-
cies (further speciation or extinction) (Bock, 2004; Roux et al., 2016).
Inference of speciation depends on different properties that are
expressed during separate evolution, such as morphological distin-
guishability, reproductive isolation and monophyly. These properties
remain the best lines of evidence to identify lineage divergence and
thus delimit species taxa (de Queiroz, 2005a,b, 2007). However, the
evolution of these properties is context dependent and can emerge
at different times and sequential order, if at all (de Queiroz, 2005a,
2007). Consequently, there is no particular property that would uni-
versally delimit a species. Not surprisingly, difficulties inherent to
species delimitation prompted proliferation of species delimitation
methods based on different premises (Fontaneto, Flot, & Tang,
2015; Raxworthy, Ingram, Rabibisoa, & Pearson, 2007; Sites & Mar-
shall, 2003, 2004), whose accuracy depended on the context of spe-
ciation (Dellicour & Flot, 2015). Furthermore, species taxa delimited
with these methods should be considered merely as scientific
hypotheses of separately evolving entities (Hey et al., 2003; de
Queiroz, 2007), which are iteratively tested using new methods and
data in the procedure called “integrative taxonomy” (Padial, Miralles,
De la Riva, & Vences, 2010; Yeates et al., 2011). The outcome of
this conceptual and methodological development is recognition that
species taxa represent a heterogeneous set of hypotheses whose
properties are contingent with the heterogeneous nature of specia-
tion.
A central question raised by this paradigm shift is whether we
can make use of the explicit links between the speciation process
and species hypotheses. If heterogeneity in the speciation process
leads to heterogeneity among species hypotheses, can we integrate
heterogeneity in speciation into evolutionary, biogeographical and
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ET AL.
ecological research? This issue has been partly explored in the case
of ecological speciation (Schluter, 2000a, 2016; Stroud & Losos,
2016). Ecological speciation is a process where ancestral populations
diverge due to resource partitioning and is associated with pheno-
typic differentiation (Nosil, 2012; Rundle & Nosil, 2005). It takes
place when ecologically accessible resources can be evolutionarily
exploited (ecological opportunity) (Schluter, 2000b; Stroud & Losos,
2016). Ecological speciation can contribute to speciation rates and
can underlie major evolutionary events such as adaptive radiation,
but its relative importance depends on ecological opportunities that
vary in space and time (Schluter, 2016). Hence, ecological speciation
provides a mechanistic explanation between ecological opportunity
and global biodiversity patterns (Kozak & Wiens, 2016; Schluter,
2016). Further generalizations require better understanding between
environmental and speciation relationships, especially regarding spe-
ciation heterogeneity.
Over the last two decades, increased evidence emerged for spe-
ciation governed by entirely different mechanisms, leading to the so-
called sibling or cryptic species. The idea that species can evolve
similar morphologies is historical (Mayr, 1942), but the use of molec-
ular delimitation methods has now brought cryptic species to the
forefront in many research arenas (Bickford et al., 2007; Knowlton,
1993; Nygren, 2014). Indeed, we are now aware that cryptic species
are quite common (Adams, Raadik, Burridge, & Georges, 2014) and
rez-Ponce de Leo
widespread across most animal phyla (Pe n & Pou-
lin, 2016; Pfenninger & Schwenk, 2007). They even have been found
rez-Ponce de Leo
in mostly overlooked parasite (Pe n & Nadler, 2010)
and nematode species (Derycke et al., 2008), but also among the lar-
gest and heavily studied mammalian species like giraffes (Fennessy
et al., 2016). In spite of being common, they are still poorly consid-
ered in testing ecological and evolutionary theories (Beheregaray &
Caccone, 2007). It is timely to intensify research beyond the phe-
nomenological level of exploration and incorporate what we can
learn from cryptic species into biodiversity science. The aim of this
review is to propose a research agenda for fully integrating cryptic
species into biodiversity science, thereby fostering a better under-
standing of the heterogeneous role of speciation in biodiversity pat-
tern and process.
Towards this goal, we examine three interrelated facets of cryp-
tic species in respect to biodiversity science (Figure 1). First, we
reconsider and define the phenomenon of phenotypic similarity from
an evolutionary perspective. We explore three nonmutually exclusive
mechanisms explaining the lack of morphological distinguishability
among divergent lineages; that is, recent divergence, niche conser-
vatism and morphological convergence. Here, we evaluate the exist-
ing empirical evidence and suggest novel tests to better elucidate
each mechanism. Second, we review the practices in delimiting cryp-
tic species and reconsider them from a taxonomic perspective. We
explore other contingent properties of species currently used to
identify species boundaries in the absence of morphological distin-
guishability. Here, we look into the burgeoning fields of DNA taxon-
omy and integrative taxonomy (Camargo & Sites, 2013; Fontaneto
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FISER ET AL. | 615

F I G U R E 1 The three sections of a research agenda for integrating cryptic species in biodiversity science. For each section, we provide the
main topics addressed (headings) as well as quantitative information retrieved from the literature (italics). Arrows show how the three sections
are integrated into biodiversity science. The quest for causal mechanisms directs taxonomic practices. Integrative taxonomy fosters
understanding of the evolutionary mechanisms behind morphological crypsis and integration of cryptic species into biodiversity research. The
latter may in turn reveal how the three mechanisms contribute to biodiversity across space and environmental gradients

et al., 2015; Padial et al., 2010), highlighting the recurrent need for
naming species. We show how integrative taxonomy can improve
understanding of morphological cryptic evolution. Third, we discuss
how cryptic species have been integrated into biodiversity research
and, more specifically, what can be gained by incorporating different
hypotheses (or properties) of speciation into biodiversity science.
Lastly, we use these facets to identify major gaps in biodiversity
research and promising research directions towards enhancing biodi-
versity science.
The ideas discussed in this review apply to all animal phyla. To
provide data-driven evaluation regarding the current research status
on cryptic diversity, we focus (but not limit) our literature search to
the Amphipoda. Amphipods are an excellent invertebrate model for
studying morphologically cryptic species, underlying speciation and
its relationship to biodiversity science. They are species rich and
ecologically diverse, thrive in most aquatic environments, play a cru-
cial role in ecosystem function and are often used as biological indi-
cators. Importantly, they comprise numerous cryptic species within
different ecological types and thus are relatively well studied in eco-
evolutionary studies (Box 1, Figure 2).
2 | COMPILATION OF LITERATURE DATA
Cryptic species were often detected as a by-product in phylogeo-
graphic studies of amphipods. For this reason, we searched for rele-
vant articles in the ISI Web of Science using keywords (Amphipoda/
Amphipods * cryptic species), (Amphipoda/Amphipods * sibling spe-
cies) and (Amphipoda/Amphipods * phylogeography) and (Amphi-
poda/Amphipods * molecular taxonomy). The search before the year
2000 yielded no results; hence, we analysed the period between
2000 and 2015 (search was made on September 2015). All titles
were checked and duplicates removed, yielding a total of 120 arti-
cles. From this search, our review covers 122 morphological species
of amphipods or morphospecies, that is species that were delimited
on a basis of their morphological distinctness. The list of morphos-
pecies contained no subspecies. These morphospecies collectively
contained a total of 439 cryptic species. Of 122 nominal species, 13
were found to be synonyms, but the remaining 109 morphospecies
represent 304 (295–315, depending on the delimitation method of
the 439 total) cryptic species discovered for the first time. Individual
articles were searched for several categories of information that
were relevant to the three topics below (see also Supporting Infor-
mation).
2.1 | Mechanisms causing cryptic diversity
From these 120 articles, we searched for information regarding three
related hypotheses explaining the lack of morphological distinguisha-
bility, namely recent divergence, phylogenetic niche conservatism and
morphological convergence. The recent divergence hypothesis posits
that cryptic species have diverged recently and morphological differ-
entiation presently is not evident (Egea et al., 2016). Here, we anal-
ysed the distribution of age of the cryptic species using reported
estimations of node age in phylogenetic trees. Descriptive estima-
tions of age were discarded (e.g., early Miocene), which reduced the
number of relevant papers to 29.
The phylogenetic niche conservatism hypothesis (PNC) postulates
that niche evolution and hence morphological differentiation across
descendant species is constrained by selection, a phenomenon
known as morphological stasis (Bravo, Remsen, & Brumfield, 2014;
Egea et al., 2016; Smith, Harmon, Shoo, & Melville, 2011). To iden-
tify cases of cryptic species potentially matching this hypothesis, we
searched for reports of cryptic species among complexes of sister
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616 | FISER ET AL.

BOX 1 Amphipods as a model for study of cryptic species

Amphipods (Crustacea: Malacostraca: Peracarida) consist of ca. 10,000 species that are classified into six orders (Horton et al., 2016;
V€ € l€a et al., 2008). There is no comprehensive molecular phylogeny of amphipods and clade-specific phylogenetic studies indicate
aino
that morphology alone neither accurately depicts species diversity nor phylogenetic relationships (Corrigan, Horton, Fotherby, White,
& Hoelzel, 2013; Fi
ser, Sket, & Trontelj, 2008; Hou et al., 2011; Lo
€rz & Held, 2004; Verheye, Backeljau, & d’Udekem d’Acoz, 2016).
Species-level taxonomy is demanding. Amphipods do not have copulatory apparatus and the species were traditionally delimited on a
basis of different appendage shapes, body shapes and setal patterns; reproductive barriers were rarely if ever studied. Within-popula-
tion variation is often high in contrast to small between-species differences.
Amphipods thrive in most aquatic habitats and some even inhabit terrestrial habitats (Ketmaier & Pavesi, 2013) (Figure 2). Many spe-
cies (80%) are marine, living in the supralittoral zone to the hadal zone, where they represent an important part of the community (Jamie-
son, Fujii, Mayor, Solan, & Priede, 2010). About 45% of freshwater species are exclusive to groundwater (V€aino
€l€a et al., 2008), a highly
bure et al., 2006). Most
constrained environment that has long been thought to promote morphological stasis and convergence (Lefe
amphipods are benthic, however, and one order (Hyperiida) is pelagic. Benthic species display highly diverse ecologies (e.g., free-roaming
species, burrowers, tube builders, sedentary ambush predators and commensals on whales, molluscs and bryozoans) and use a broad
range of feeding strategies (e.g., filter feeding, shredding, scavenging and predation) (Alexander, Dick, & O’Connor, 2013; Macneil, Dick,
& Elwood, 1997). Local abundances can be high; hence, they are also a key link in food webs (Pinchuk, Coyle, Farley, & Renner, 2013).
Lastly, amphipods are routinely used in ecotoxicological tests (Feckler et al., 2012; Marmonier et al., 2013), the results of which may be
biased if model species contain cryptic species with different sensitivities to pollutants.
In the absence of free pelagic larvae, most amphipod species have limited distributional ranges (Myers & Lowry, 2009). Yet, some
tens of species, including some cryptic species (Cristescu, Witt, Grigorovich, Hebert, & MacIsaac, 2004; Pilgrim, Blum, Reusser, Lee, &
Darling, 2013; Pilgrim & Darling, 2010), have substantially expanded their distributional ranges in recent decades (Grabowski, Bacela,
& Konopacka, 2007; Jazdzewski, Konopacka, & Grabowski, 2004). Some amphipods are invasive species and pose a threat to native
fauna (Dick & Platvoet, 2000; Dodd et al., 2014).
Amphipods are an ideal model organism for linking evolutionary processes contributing to cryptic diversity with local ecological
dynamics, global biodiversity patterns and applied ecology. Cryptic species have been found in all ecological groups of amphipods.
The number of cryptic species within nominal species varies up to several tens of species (Havermans, 2016; Katouzian et al., 2016;
Mamos et al., 2016; Witt et al., 2006). Ecological diversity of amphipods allows for testing generalities in processes generating cryptic
diversity under different ecological settings. Limited distributional ranges at the species level coupled with ubiquitous distribution at
the genus level provide natural replicates for analysis. As a key functional group in ecosystems, amphipods naturally link the issue of
morphological evolution with local ecological dynamics, ecosystem functioning and nature conservation.

species that were ecologically specialized at the microniche level.
We assumed that a single origin of narrow specialization in an ances-
tor parsimoniously explains specialization in sister descendants more
than multiple and independent origins.
The morphological convergence hypothesis also is based on selec-
tion and assumes that morphological similarity may evolve indepen-
dently among distantly related species in response to similar
selection pressures (Bravo et al., 2014; Trontelj et al., 2009). Here,
we explored whether morphological similarity of cryptic species
evolved independently through convergent evolution. For this rea-
son, we quantified the proportion of cryptic species that were not in
sister relationships with each other.
2.2 | Taxonomic practices in delimiting cryptic
species
Authors rarely a priori referred to a well-defined species concept
while delimiting species taxa. For this reason, the evaluation what
they considered as a species was not possible. The following analysis
of past research is based on the premise that species are separately
evolving entities and that species taxa can be delimited using the cri-
teria of genetic isolation.
We reviewed the number and type of molecular markers as well
as the methods used to delimit cryptic species. Molecular markers
included allozymes, mitochondrial and nuclear genes, microsatellites
and single nucleotide polymorphisms (SNPs). DNA taxonomy is a
rapidly evolving field such that molecular methods for species delimi-
tation used a decade ago may not be considered valid today (com-
pare, e.g., the classifications of Sites & Marshall, 2004, 2003 and
Flot, 2015; Fontaneto et al., 2015). All methods, albeit on different
premises, search for cessation of gene flow between populations.
Such genetic isolation is a primary pointer of ongoing speciation
(Bock, 2004) and emergence of independently evolving entities (de
Queiroz, 2007) and serves for delimitation of corresponding species
taxa (see Glossary). The progress in methodology makes any classifi-
cation using different methods a difficult exercise. For this review,
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FISER ET AL. | 617

F I G U R E 2 (as part of Box 1). A

snapshot of Amphipoda diversity.
Lyssianasoids (a) live in the deep sea at
depths below 5000 m depth; ampeliscids
(b) commonly burrow in soft sediments;
corophiids (c) are filter feeders that live in
self-built tubes; caprellids (d) mimic plants
on which they live; leucothoids (e) and
cyamids (f), respectively, live in association
with sponges and whales; several lines of
talitroids (g) successfully colonized
semiterrestrial supralittoral habitats, while
hyperiids (h) live pelagial, often within
gelatinose plankton. Cryptic species were
found in all these ecological groups. They
naturally pose the question whether the
relative importance of evolutionary
mechanisms underlying morphological
crypsis differs across ecological settings. All
photographs made by Hans Hillewaert and
used with permission (licensed under
Creative Commons, photos available at
https://www.flickr.com/photos/bathypore
ia/albums/72157639365477036)

we used four categories for classification: namely, distance-based,
tree-based, allele sharing and population genetics methods (Table 1).
Distance-based methods assume that speciation should result in
smaller genetic distances within than between species. Species are
bure, Douady, Gouy, &
delimited either using a fixed threshold (Lefe
Gibert, 2006) or the best-fitting threshold calculated for the data set
at hand (Puillandre, Lambert, Brouillet, & Achaz, 2012). Tree-based
methods search for the most likely transition point between species-
level and coalescent processes using single locus (Monaghan et al.,
2009; Pons et al., 2006; Reid & Carstens, 2012; J. Zhang, Kapli, Pav-
lidis, & Stamatakis, 2013), multiple loci (Ence & Carstens, 2011;
Grummer, Bryson, & Reeder, 2014; Knowles & Carstens, 2007;
O’Meara, 2010; Yang & Rannala, 2010, 2014) and genomic-scale
data (Leache, Fujita, Minin, & Bouckaert, 2014). Allele sharing-based
€ rheide, & Datta-
methods (Flot, Couloux, & Tillier, 2010; Flot, Wo
gupta, 2010) attempt to discern populations that are no longer
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618 | FISER ET AL.

T A B L E 1 Classification of methods used in DNA taxonomy to delimit cryptic species of amphipods

Methods Delimitation criteria
Distance-based methods Intraspecific genetic variation

interspecific variation
Tree-based methods Point of transition from species-level
to population-level processes
Allele-sharing based Mutual allelic exclusivity
Population genetics Reduced gene flow among populations
Examples of analyses/programmes
Fixed molecular threshold, automated
barcoding gap detection
GMYC, PTP, BP&P, BFD, BFD*,
SpedeSTEM, Brownie
Haplowebs
Nested clade analysis,
differentiation statistics
References
bure et al. (2006),
Lefe
Puillandre et al. (2012)
Pons et al. (2006), O’Meara (2010),
Ence & Carstens (2011), Grummer et al.
(2014), Yang & Rannala (2010),
Flot, Couloux, et al. (2010), Flot,
Wo € rheide, et al. (2010)
Delimit differentiated populations
rather than species

GMYC, Generalized mixed Yule-coalescent models; PTP, Poisson tree processes models; BP&P, Bayesian phylogenetics & phylogeography; BFD, Bayes
factor delimitation (BFD* for genomic-scale data).

connected by gene flow and therefore evolved mutual allelic exclu-
sivity. We recognize that population genetic methods (e.g., nested
clade analysis, indices of genetic differentiation) are not intended to
solely delimit species, but have been used often in the past in
respect to species delimitation. In fact, many authors considered
genetically distinct populations as putative species.
In addition, we quantified cases when cryptic species were anal-
ysed for differences in morphology, physiology, ecology or beha-
viour. Compositing different data types to delimit species is known
as integrative taxonomy (Padial et al., 2010; Wiens & Penkrot,
2002). It can either provide additional support for a species hypothe-
sis (Schlick-Steiner et al., 2010) or detect contradictions among data
(Padial et al., 2010); both help link taxonomy with evolutionary biol-
ogy (Sites & Marshall, 2003, 2004). Finally, we examined whether
cryptic species have a binomial name and, if so, it is based solely on
€rger &
molecular criteria (Cook, Edwards, Crisp, & Hardy, 2010; Jo
€ dl, 2013; Renner, 2016). Although naming is not always done,
Schro
the naming of new species integrates taxonomy with other fields of
biology (Pante, Schoelinck, & Puillandre, 2015).
Berns, Kozak, and Wiens (2009) and Harmon, Schulte, Larson, and
Losos (2003) for changes in morphology through time). The evolu-
tion of morphological distinctness depends only on time since diver-
gence; hence, cryptic species are expected to be relatively young
n
(Zu ~ iga-Reinoso & Benıtez, 2015). Diagnostic morphological traits
evolve slowly if they are selectively neutral, effective population size
is large and ancestral polymorphism is high (Egea et al., 2016; Wiens
& Servedio, 2000).
We obtained age estimates for 43 cryptic species of amphipods
(Figure 3). The age distribution was typically skewed left, but only
five of the 43 cryptic species were younger than 1 Myr. This result
is in stark contrast to theoretical predictions mentioned above. One
explanation may be that this mechanistic explanation is unlikely. The
evolutionary response to environmental selection is rapid (Carroll,
Hendry, Reznick, & Fox, 2007; Herrel et al., 2008); thus, evolving
species quickly attain their morphological distinctness. The alterna-
tive explanation invokes methodological biases. First, the methods
used for age estimation have (and are still ongoing) changed over
time, and current estimated ages are sensitive to a number of poorly
understood parameters (dos Reis, Donoghue, & Yang, 2015).

2.3 | Cryptic species in biodiversity research

Although cryptic species are being documented at an ever-increasing
rate, they are integrated in quite different ways across fields in bio-
diversity science. Here, we distinguish between two major ways of
incorporating cryptic species in biodiversity research. The first corre-
sponded to studies that explore whether cryptic species might have
biased our understanding of biodiversity patterns and thus misled
conservation efforts. The second corresponded to studies that only
retain DNA-based criteria for delimiting species, thereby inherently
using cryptic species as units of analysis.

3 | MECHANISMS CAUSING CRYPTIC

DIVERSITY

3.1 | Recent divergence F I G U R E 3 Age distribution of 43 cryptic species of amphipods,

extracted from 29 of 120 reviewed publications. Please note that
The simplest evolutionary model predicts that morphological dispar- the methods used for estimation of divergence vary between
ity increases due to stochastic processes alone (see, e.g., Adams, studies, see text



FISER ET AL.
Different authors estimated node ages using different methods, opti-
mized for their data sets. Some variation in age estimation among
these studies is unavoidable and at times even biased. Second, many
evolutionarily young cryptic species might have been simply over-
looked. Most of the reviewed studies used coarse delimitation meth-
ods that accurately delineate only relatively old species (see
Section 3). Consequently, we conclude that recent divergence pre-
sently explains morphological similarity of only a small fraction of
known cryptic species.
To note, none of the examined studies explicitly tested for recent
divergence. This hypothesis has two central predictions: first, cryptic
species are young and, second, morphological traits evolve under the
neutral model of evolution (Brownian motion, see Glossary) (Felsen-
stein, 1985). Rigorous testing of the predictions should consider
three aspects as guidelines for future research. First, testing requires
accurate age estimations. This task is not easy and methodological
details are beyond the scope of this review; readers should consult
more specialized papers (dos Reis et al., 2015). Second, the distinc-
tion between “young” and “old” species depends on ancestral poly-
morphism and population size; therefore, it is clade specific.
Appropriate evaluation of the hypothesis needs to account for clade
specificity. For instance, assessing whether cryptic species are
younger than noncryptic ones requires analysis at the clade level
rather than the species pair level. Lastly, models of evolution can be
estimated from extant morphology and phylogeny, but a changing
selection regime also can produce a pattern similar to neutral evolu-
tion and thus lead to erroneous estimation of trait evolution. Fortu-
nately, this issue can be solved using recently developed software
that allows for discrimination between models of neutral evolution
and changing selective regimes (Clavel, Escarguel, & Merceron,
2015).
3.2 | Phylogenetic niche conservatism (PNC)
Recent divergence cannot explain relatively old cryptic species. An
alternative hypothesis, the so-called morphological stasis, assumes
that morphological differentiation of descendant species is con-
strained by biological mechanisms (Bickford et al., 2007). As a spe-
cies’ morphology is partly related to its ecological niche (e.g., Losos,
2009; Schluter, 2000a), this hypothesis is closely related to the
broader concept of phylogenetic niche conservatism (PNC). Initially,
PNC was used to explain the tendency for some lineages to retain
their ecological niches over evolutionary time. More recently, the
concept was elaborated further (Pyron, Costa, Patten, & Burbrink,
2015), but here we refer to its original intention. The biological
mechanisms underlying PNC encompass stabilizing selection, gene
flow swamping local adaptation, pleiotropic effects constraining
adaptation and lack of genetic variation (Losos, 2008; Wiens, 2004,
2008; Wiens & Graham, 2005; Wiens et al., 2010).
The PNC hypothesis was not explicitly tested in the reviewed
studies here. Nevertheless, we found several cases of cryptic species
among complexes of sister amphipod species that were ecologically
highly specialized and might support the PNC hypothesis. These
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| 619
include Cyamus species (whale lice) living on distinct parts of a
whale’s body (Kaliszewska et al., 2005), Niphargus species colonizing
fissures in rock (Fi
ser & Zagmajster, 2009; Meleg, Zak
sek, Fi
ser,


Kelemen, & Moldovan, 2013; Svara, Delic, Rada,
 & Fi
ser, 2015;
Trontelj et al., 2009), some species of Gammarus inhabiting mountain
streams (Hou & Li, 2010) and sponge-dwelling species of Leucothoe
(Richards, Stanhope, & Shivji, 2012; White, Reimer, & Lorion, 2016).
This list is likely longer, especially among deep sea and subterranean
amphipods. Regardless, attributing morphological crypsis to PNC for
species with unclear ecological specialization is problematic in the
absence of explicit testing.
We now discuss three predictions of the PNC to stimulate future
research regarding mechanisms causing cryptic diversity (Pyron et al.,
2015; Wiens et al., 2010). First, evolution of morphology is con-
strained. Morphological disparity remains constant through time, as
if being constrained by stabilizing selection. The model of morpho-
logical evolution inferred from extant morphology and phylogeny no
longer corresponds to neutral Brownian motion but to models simu-
lating non-neutral evolution (but see Losos, 2008). These models
include stabilizing selection (Orstein-Uhlenbeck model, see Glossary)
or, arguably, constantly moving adaptive optima (white noise model,
see Glossary) (Pyron et al., 2015; Smith et al., 2011; Wiens et al.,
2010). The preferred models are selected based on likelihood values.
Some authors proposed an alternative test using a special model of
Brownian motion that allows for different rates of trait evolution
across clades. The rates of trait evolution should be lower in niche-
, San-
conserved than in niche nonconserved clades (O’Meara, Ane
derson, & Wainwright, 2006; Wiens et al., 2010). Second, sister
cryptic species are expected to share ecological niches. Equivalency
among ecological niches can be tested either implicitly from distribu-
tional data (Kozak & Wiens, 2006; Raxworthy et al., 2007; Warren,
Glor, & Turelli, 2008) or from experimental data (Kearney, Wintle, &
Porter, 2010). Third, PNC promotes allopatric speciation (Kozak &
Wiens, 2006; Pyron et al., 2015; Wiens, 2004; Wiens & Graham,
2005). This prediction requires analysis of the evolution of geo-
graphic ranges (Matzke, 2013; Ree & Smith, 2008). To note, the
third prediction may strengthen arguments supporting PNC, but it is
not mandatory. Species can evolve in sympatry along niche axes, for


example salinity, pH or temperature (Delic, Svara, Coleman, Trontelj,
& Fi
ser, 2017) that are not related to morphology.
3.3 | Morphological convergence
The third hypothesis infers that morphological similarity evolved
among distantly related species in response to similar selective
regimes (Ingram & Mahler, 2013). Morphological convergence based
on our reviewed data was common: 26% of the nominal amphipods
examined contained cryptic species that were not sister groups. This
proportion is probably a low estimate because detection of conver-
gence depends on completeness of taxon sampling. Cases of mor-
phological convergence among cryptic species were documented in
several amphipod genera, where species from the same cryptic com-
plex independently colonized freshwater-semiterrestrial (Yang, Hou,

620 | FISER
& Li, 2013) or subterranean habitats (Villacorta, Jaume, Oromı, &
Juan, 2008) or microhabitats within the subterranean realm (Trontelj,
Blejec, & Fi
ser, 2012; Trontelj et al., 2009).
Evidence from the above studies is descriptive. A central predic-
tion of this hypothesis states that convergent evolution should result
from shifts in selective regimes. Appropriate testing must show a
correlated evolution between morphology and the environment. The
evolution of morphology should correspond to the Ornstein–Uhlen-
beck stabilizing selection model (see Glossary) (Butler & King, 2004;
Hansen, 1997). Further, Ingram and Mahler (2013) developed a
method to map shifts in continuous phenotypic characters towards
convergent regimes on a phylogenetic tree and to test whether
these shifts are more numerous than expected under a given null
model.
3.4 | General summary of invisible species
diversification
Patterns of cryptic species, that is the distribution of cryptic species
across space and taxa as well as the occurrence of closely related/
distantly related cryptic species, have been relatively well docu-
mented in the amphipod literature and in the literature in general.
Yet, there is comparatively much less knowledge about the relative
importance of different mechanisms generating cryptic species. As
usual in science, patterns alone are not enough to infer mechanism
(i.e., different mechanisms can generate the same pattern), there is a
need for a shift from pattern-oriented studies of cryptic diversity to
mechanism-oriented studies of cryptic diversity. The mechanisms
generating cryptic species are clearly diverse. They likely follow the
same evolutionary and ecological principles that generated the diver-
sity of morphologically distinguishable species and have fascinated
naturalists for centuries (Collar, Schulte, & Losos, 2011; Harmon
et al., 2010; Losos, 2011; Nosil, 2012). The lack of morphological
diversification is an evolutionary phenomenon, a counterpart to the
long-studied mechanisms of morphological diversification such as
character displacement (Schluter, 2000a; Stuart & Losos, 2013).
Research on morphological similarity is hence closely related to that
on morphological diversification. It requires gathering information on
the function and heritability of traits as well as on how trait variation
relates to fitness (Schluter, 2000a; Stuart & Losos, 2013). Contrary
to morphological diversification, mechanisms causing morphological
similarity have received little attention. Most of the reviewed studies
focused on revealing cryptic species but did not test for causal
mechanisms. Thus even if slightly morphologically different, any spe-
cies pair satisfying the predictions above might be treated as mor-
phologically cryptic.
Many authors stated that perfect morphological similarity does
not exist and that morphological analyses based on molecular spe-
cies delimitation often yield morphological distinctness. Hence, some
researchers consider the concept of cryptic species as overrated
(Jugovic, Jal
zic, Prevor
cnik, & Sket, 2012; Karanovic, Djurakic, &
n
Eberhard, 2016; Knowlton, 1993; Zu ~iga-Reinoso & Benıtez, 2015).
Noteworthy, some authors have already coined a term “pseudo-
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ET AL.
cryptic” to distinguish “completely identical species” from “morpho-
us, 2015;
logically diagnosable species” (Achurra, Rodriguez, & Erse
Knowlton, 1993; Saez & Lozano, 2005). This classification may lead
to questions such as “When are species similar enough to be consid-
ered morphologically cryptic?” (Karanovic et al., 2016; Lajus, Sukhikh,
& Alekseev, 2015). This question is at risk to remain without epi-
logue. Importantly, it could hinder exploration of a rather broadly
widespread evolutionary phenomenon and even impede progress in
biodiversity science. As discussed further below, the quest for mech-
anisms can lead taxonomic practices towards delivering species
hypothesis that are theoretically grounded in the heterogeneous
properties of speciation (Section 3) and can better integrate the spe-
ciation process into ecology and evolution (Section 5).
4 | TAXONOMIC PRACTICES IN
DELIMITING CRYPTIC SPECIES
4.1 | Species delimitation methods
Up to now, most cryptic species of amphipods were delimited using
either one or two genes (Figure 4a). The mitochondrial cytochrome
oxidase subunit I (COI) gene was used in 83% of the reviewed stud-
ies, possibly reflecting the general use and applicability of this mar-
ker across most animal phyla (Hebert, Cywinska, Ball, & DeWaard,
2003; Hebert, Ratnasingham, & Waard, 2003) and as a well-devel-
oped “barcoding” system for storage and identification of animal spe-
cies (Ratnasingham & Hebert, 2007). Other genetic markers included
allozymes, additional mitochondrial markers (16S and CytB) and
nuclear markers (28S rDNA, ITS, H3, EF1a, ND II and 18S rDNA).
Guerra-Garcıa et al. (2006) used RAPDs to explore intra- and inter-
specific genetic differentiation in two species of caprellidean amphi-
pods. Microsatellites were developed for numerous amphipods
(Baird, Miller, & Stark, 2012; Rewicz, Wattier, Rigaud, Bacela-Spy-
chalska, & Grabowski, 2015; Villacorta, Canovas, Oromi, & Juan,
2009; Weiss & Leese, 2016), but were never used for taxonomic
purposes and are not considered here.
Molecular delimitation of cryptic amphipod species most often
relied on a single category of methods; only 30% of the examined
studies combined two or three methods (Figure 4b). In most studies,
species were delimited using distance-based methods or using a com-
bination of distance-based and population genetics methods (Fig-
ure 4b). There was a substantial lag in the application of tree-based
methods. The generalized mixed Yule-coalescent (Pons et al., 2006),
multilocus coalescent (Rannala & Yang, 2003; Yang & Rannala, 2010)
and Poisson tree process models (Zhang et al., 2013) were used in
only seven studies (Copilasß-Ciocianu & Petrusek, 2015; Esmaeili-
Rineh, Sari, Delic, Mo
skri
c, & Fi
ser, 2015; Katouzian et al., 2016; King
& Leys, 2011; Murphy, King, & Delean, 2015; Weiss, Niklas, Anna, &
Florian, 2014; Yang et al., 2013). This lag in the use of tree-based
methods occurred despite 78% of the studies inferring molecular phy-
logenies (supporting information 1). Allele sharing-based methods, for
example haplowebs (Flot, Couloux, et al., 2010), were used in only
two studies (Brad, Fi
ser, Flot, & Sarbu, 2015; Flot et al., 2014).



FISER ET AL.
F I G U R E 4 An overview of practices in taxonomy to delimit
cryptic species of amphipods. (a) Number of molecular markers
(n = 76 studies); (b) Molecular methods to species delimitation
(n = 76 studies); (c) Nonmolecular data used to test cryptic species
hypotheses inferred from DNA taxonomy (n = 55 described species
containing cryptic species complexes)
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| 621
Use of different molecular markers and species delineation
methods revealed conflicting results about the number of species.
Alternative species delimitations suggested by different methods
were not in conflict with each other, but differed in the degree of
splitting; distance methods typically turned to be more conserva-
tive (Copilasß-Ciocianu & Petrusek, 2015; Delic, Trontelj, Rendo
s, &


Fi
ser, 2017; Delic, Svara, et al., 2017; Eme et al., 2017; Katouzian
et al., 2016; Weiss et al., 2014). In such cases, authors either pro-
vided a rough estimate of species number (Copilasß-Ciocianu & Pet-
rusek, 2015; Weiss et al., 2014), opted for a particular species
hypothesis by ranking the efficiency of different methods (e.g.,
conservative ABGD was preferred over PTP and bGMYC; Katou-
zian et al., 2016), reconsidered the results within spatial context
(presence of syntopy (Delic, Trontelj, et al., 2017)) or drew on
other studies to justify the choice of a particular threshold value.
Unfortunately, cross-referencing is not always appropriate because
the value of thresholds depend on how genetic distances are cal-
culated (e.g., uncorrected p, K2P, patristic distances) (Richards
et al., 2012). Moreover, the use of thresholds is case-specific
because the rate of substitution differs among taxa (but see
bure et al., 2006). Oddly, reasons for the discordant number
Lefe
of species number were never explicitly addressed. Inconsistency
among different species delimitation methods is well known, aris-
ing due to violations of various assumptions required by the dif-
ferent delimitation methods (Carstens, Pelletier, Reid, & Satler,
2013). Molecular species delimitation methods generally yield con-
gruent results when speciation rates are low, population sizes are
small, and the molecular markers used have a high mutation rate
(Dellicour & Flot, 2015; Fontaneto et al., 2015). On the contrary,
evolutionarily young species with large effective population sizes
can be a source of dispute (as alluded to above). A highly promis-
ing solution for the issue seems to be genomewide multilocus coa-
, Burbrink, McGuire, & Moritz, 2012;
lescence (Fujita, Leache
Leache et al., 2014), and also confrontation with nonmolecular
characters as discussed in the next section.
4.2 | Confronting species criteria
Ideally, species should be delimited using an integrative approach
including genetics, morphology, ecology, behaviour and geography
(Edwards & Knowles, 2014; Guillot, Renaud, Ledevin, Michaux, &
Claude, 2012; Padial et al., 2010). Steps towards integrative taxon-
omy were made in 55 of the 122 (42%) nominal species examined.
To note, integrative exploration of cryptic species complexes often
occurred in a series of consecutive publications by a research group.
Molecular inferences were mostly supplemented with morphological
and ecological data as well (Figure 4c). Reproductive barriers were
explicitly inferred from mating behaviour in five cryptic species com-
plexes. Differences in genome size were reported for a single species
complex. No biological difference between cryptic species, except
genetic ones, was detected in only four of the 55 nominal species
(Cothran, Henderson, Schmidenberg, & Relyea, 2013; Meleg et al.,
2013; Wellborn & Cothran, 2004).
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622 | FISER ET AL.

4.3 | Naming cryptic species

In most cases, cryptic species were un-named, even when supported
by multiple lines of evidence. The 304 (295–315 depending on the
method, excluding nominal species) species of amphipods discovered
in the period 2000–2015 represented 17% of the 1822 amphipod
species described during the same time period (Figure 5). Yet, only
21 of these cryptic species were described and named. In other
words, DNA-complemented taxonomy contributed only 1% to the
total number of described amphipod species. Only two studies relied
solely upon DNA sequences to diagnose species (Delic, Trontelj,
et al., 2017; Murphy et al., 2015), and one study complemented
morphological diagnoses with diagnostic COI sequences (King &
Leys, 2011).

4.4 | Future challenges for the taxonomy of cryptic

species
Taxonomic practices can contribute more to the mechanistic under-
standing of morphological crypsis as well as to the integration of
cryptic species into biodiversity research. Aside from technical issues
re et al., 2017),
such as development of barcoding libraries (Morinie
we envision three important issues.
First, testing whether cryptic species are evolutionarily young
requires using species delimitation methods that are sensitive
enough to detect early divergence, for example before evolving spe-
cies reach reciprocal monophyly. Lineage sorting can take a long
time in species with large population sizes (Dellicour & Flot, 2015;
Knowles & Carstens, 2007). Haploweb and multilocus coalescent
methods are both designed to delimit nonmonophyletic species. A
major impediment to broaden implementation of the two methods is
the low number of nuclear markers exhibiting both suitable variabil-
ity and low homoplasy (Kornobis & Palsson, 2011, 2013; Nahavandi,
Ketmaier, & Tiedemann, 2012). Among amphipods, only two markers
€rheide, et al.,
(ITS, EF1a) apparently meet these conditions (Flot, Wo
2010; Nahavandi et al., 2012). Fortunately, high-throughput
sequencing technologies are becoming readily accessible and afford-
able; thus, multilocus species delimitation may become standard F I G U R E 5 Rates of species description and discovery of cryptic
within the next few years (Raupach, Amann, Wheeler, & Roos, 2016) species of amphipods. Upper panel shows rates of species
and the recent divergence hypothesis may increase in importance (see description between 2000 and 2015 (source: Amphipoda
Section 3.1). Newsletters vol. 30–39). Middle panel shows cryptic species
discovery rate (source Supplementary Information) over the same
Second, taxonomy can strengthen the link between species
time period. Lower panel shows that the proportion of discovered
hypotheses and the speciation process or, more generally, between
but undescribed cryptic species increases through time
taxonomic practice and evolutionary theory (de Queiroz, 2007). Only
practices grounded in theory can fully appreciate the heterogeneous (Herrel et al., 2008) can increase taxonomy rigour. Some taxonomists
nature of speciation, and appropriately confront multiple data (mor- consider species hypotheses supported by multiple lines of evidence
phology, ecology, physiology, multiple DNA) to unveil the full spec- as more robust than single line evidence (Padial et al., 2010). Yet
trum of divergent processes. This strengthening is a major step incongruences among data can yield species hypotheses as robust as
towards discovery of general rules in the speciation process (Butlin those supported by congruence as long as incongruences have
et al., 2012) and linking speciation with other fields in biodiversity sound evolutionary explanations.
science (Section 5). Further, understanding why some lineages genet- Third, novel species, no matter if morphologically cryptic, can be
ically diverge without morphological difference, or conversely, why € rger & Schro
described and named (Jo € dl, 2013; Pante et al., 2015).
some genetically nearly identical populations ecologically differ This practice is one way to communicate cryptic species with other



FISER ET AL.
fields of biodiversity science that use Linnaean binomials in their
research. It is paradoxical that cryptic species remain nameless until
described based on morphological criteria. Finding morphological
diagnostic traits among morphologically cryptic species is challenging
(Fi
ser & Zagmajster, 2009; Schlick-Steiner et al., 2010) and the prac-
tical value of such diagnoses may be questionable (Jugovic et al.,
2012). Indeed, The International Code of Zoological Nomenclature
(http://iczn.org/code, ICZN) does not limit the diagnosis of species
to the use of morphological traits. The idea of diagnosing species
using DNA sequences is not new (Goldstein & DeSalle, 2011;
Knowlton, 1993), but descriptions relying only on molecular data are
generally still rare (Clouse & Wheeler, 2014; Cook et al., 2010;
Edgecombe & Giribet, 2008; Halt, Kupriyanova, Cooper, & Rouse,
€ rger & Schro
2009; Harvey, Berry, Edward, & Humphreys, 2008; Jo €dl,
2013; Murphy et al., 2015; Renner, 2016; Strand & Sundberg,
2011). All these studies broadly agree that holotypes should be
defined and deposited into collections. Technical aspects vary on
how species are diagnosed (Goldstein & DeSalle, 2011; Renner,
2016), and recent works recommend two technical details. First,
diagnosis should rely on diagnostic substitutions rather than genetic
distances (i.e., nodes in phylogeny). Second, detailed alignment con-
struction, sequences and final alignments must be made available to
€rger & Schro
ensure repeatability and continuity in taxonomy (Jo €dl,
2013; Renner, 2016). An important corollary of the molecular
description of cryptic species is that species retaining the original
name need to be molecularly diagnosed as well. This step may
require designation of neotypes or co-types that can replace or sup-
plement holotypes if the latter are lost or improperly preserved for
DNA analysis. Finally, formal naming sometimes is not considered
desirable when species hypotheses need to be strengthened with
additional lines of evidence of lineage separation. In such cases,
Morard et al. (2016) proposed an interim nomenclature system to
codify genetically circumscribed entities, including potential cryptic
species, as an effort to communicate data on genetic diversity for
multiple biodiversity stakeholders. Presently, we can only acknowl-
edge that the majority of cryptic species uncovered by DNA taxon-
omy remains silent to biodiversity research.
5 | CRYPTIC DIVERSITY IN BIODIVERSITY
RESEARCH
5.1 | Biodiversity patterns revisited and
consequences for nature conservation
Following the plea by Bickford et al. (2007) to account for cryptic
species in biodiversity science, we now revisit a number of biodiver-
sity-related issues. Notably, the number of examined studies strongly
depended on the scale of the analysis.
5.1.1 | Global-scale analyses
Global-scale analyses are few. Pfenninger and Schwenk (2007) con-
ducted a meta-analysis of cryptic species to test for variation in the
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| 623
proportion of cryptic species across major metazoan phyla and bio-
geographical regions. The authors found that cryptic species were
homogeneously distributed among taxa and regions and concluded
“that cryptic metazoan diversity can be treated as random error in
biodiversity assessments.” Their meta-analysis was later criticized for
several methodological problems (Trontelj & Fi
ser, 2009), and addi-
tional analyses almost a decade later suggested that cryptic species
actually may be heterogeneously distributed across animal phyla
rez-Ponce de Leo
(Pe n & Poulin, 2016). The evidence for homoge-
nous distribution of cryptic species across geographic regions is con-
flicting (Eme et al., 2017; Gill et al., 2016; Voda, Dapporto, Dinca, &
Vila, 2015); perhaps an heterogeneous distribution can be detected
only at global geographic scales.
Finding that cryptic species are homogeneously distributed
across space does not necessarily imply that the mechanisms causing
cryptic species are themselves invariant. These mechanisms can
compensate each other across space to produce an even distribution
of cryptic species. An untested hypothesis is that selectively neutral
mechanisms (e.g., the recent divergence hypothesis) predominate in
regions where recent climatic perturbations fragmented ranges of
ancestral species (e.g., Pleistocene glaciations, Fi
ser et al., 2010),
whereas selection-based mechanisms (PNC, morphological conver-
gence) operate more frequently in environments with strong direc-
tional selection (Bickford et al., 2007; Trontelj & Fi
ser, 2009).
It also is unclear why cryptic species are overrepresented in
some phyla. Knowlton (1993) suggested that cryptic species may be
more frequent in taxa that do not rely on visual information, but we
are not aware of a single study that explicitly addressed this ques-
tion. Analogous to geographic aspects of cryptic diversity, the rela-
tive importance of the three mentioned mechanisms causing
morphological crypsis in different taxonomic groups awaits to be
quantified and explained. In particular, PNC may well explain the
morphological similarity in organisms, the taxonomy of which has
been based on functional somatic characters related to ecology (e.g.,
amphipods: Dahl, 1977; Fi
ser, Trontelj, Lu
strik, & Sket, 2009). In con-
trast, it may be less important in species delimited essentially on sex-
ual characters, such as isopods or spiders.
5.1.2 | Geographically and phylogenetically limited
analyses
Most studies are limited either in geographic or phylogenetic scope.
In the amphipod literature, these include but are not limited to a
species geographic range size (Trontelj et al., 2009), the extent of
ecological niche overlap and species coexistence (Fi
ser, Altermatt,
Zak
sek, Knapi
c, & Fi
ser, 2015), the strength of size-assortative pair-
ing (Galipaud et al., 2015), the effectiveness of conservation mea-
sures (Venarsky, Anderson, & Wilhelm, 2009) and the use of
biological indicators in ecosystem health assessment (Feckler, Schulz,
& Bundschuh, 2013; Feckler, Thielsch, Schwenk, Schulz, & Bund-
schuh, 2012; Feckler et al., 2014; Major, Soucek, Giordano, Wetzel,
& Soto-Adames, 2013; Soucek, Dickinson, Major, & McEwen, 2013;
Weston et al., 2013; Zettler et al., 2013). Notably, all these studies

624 | FISER
consider cryptic species as a source of error that must be accounted
for when documenting and explaining biodiversity patterns.
The question of whether the range size of cryptic species is
smaller than that of corresponding morphological species was
addressed explicitly in amphipods from Antarctic deep sea (Baird
€ rz, Maas, Linse, & Coleman, 2009), desert springs
et al., 2012; Lo
Australia and North America (Murphy, Adams, Guzik, & Austin,
2013; Witt, Threloff, & Hebert, 2006) and groundwater amphipods
from Australia, Canary Islands and Europe (e.g., Bauza-Ribot, Jaume,
 s, Juan, & Pons, 2011; Bradford, Adams, Humphreys, Austin, &
Forno
Cooper, 2010; Bradford et al., 2013; Meleg et al., 2013; Trontelj
et al., 2009; Villacorta et al., 2008). In general, large range sizes of
morphological species were “symmetrically” divided into a series of
smaller ranges for cryptic species. Yet, some studies reported “asym-
metrical” fragmentation where the range of at least one cryptic spe-
cies was as large as that of the morphological species (Havermans,
bure et al., 2006).
Nagy, Sonet, De Broyer, & Martin, 2011; Lefe
Whether symmetrical and asymmetrical fragmentations of morphos-
pecies ranges are homogeneously distributed across geographic
regions has yet to be determined. One study indicates, however,
that consideration of cryptic species does not affect continental
scale patterns of range size, the so-called Rapoport effect (i.e., the
pattern of increasing range size of morphological species at higher
latitudes in the Palearctic region; Stevens, 1989) (Eme et al., 2017).
Another important aspect is whether morphologically cryptic spe-
cies have the same ecological requirements (i.e., Grinnellian niche)
and play similar roles in ecosystems (i.e., Eltonian niche) (Fi
ser et al.,
2015). Almost all detailed ecological studies showed that cryptic spe-
cies differed in their requirements along one or more dimensions of
their Grinnellian niche (Colson-Proch, Renault, Gravot, Douady, &
Hervant, 2009; Eisenring, Altermatt, Westram, & Jokela, 2016;
€rss, Zettler, & Bas-
Krebes, Blank, & Bastrop, 2011; Krebes, Blank, Ju
trop, 2010; Rock, Ironside, Potter, Whiteley, & Lunt, 2007). Appar-
ently, cryptic species may not be cryptic to other community
members. Studies on cryptic Hyalella species imply different vulnera-
bilities to fish predation (Cothran, Henderson, et al., 2013; Wellborn
& Cothran, 2004, 2007). Westram, Baumgartner, Keller, and Jokela
(2011) showed different susceptibilities to acanthocephalan parasites
among cryptic species of the Gammarus fossarum species complex,
and Colson-Proch et al. (2009) found substantial differences in beha-
vioural, metabolic and biochemical responses to cold among cryptic
species of the subterranean amphipod Niphargus rhenorhodanensis.
Ecotoxicological tests further revealed large differences in sensitivity
to a number of pollutants across a range of cryptic taxa (Feckler
et al., 2012, 2013, 2014; Major et al., 2013; Soucek et al., 2013;
Weston et al., 2013). Interpretation of the magnitude of these differ-
ences in an ecological context is highly challenging, but studies on
co-occurrence of cryptic species indicate they are insufficient to
mediate stable coexistence (Box 2).
Cryptic species having a roughly similar role in the ecosystem
(Eltonian niche) but differing in their environmental requirements
and responses to various stressors may be functionally redundant. If
so, cryptic species may be critically important in stabilizing
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ET AL.
ecosystem functioning (Elmqvist et al., 2003; Harvey, Gounand,
Ward, & Altermatt, 2017; Scheffer et al., 2015). To our knowledge, a
single study using cryptic nematodes as a model system explored
differences in the functional role of cryptic species (De Meester,
Gingold, Rigaux, Derycke, & Moens, 2016). A microcosm experiment
by these authors unveiled species-specific effects on organic matter
decomposition, challenging the hypothesis of functional redundancy.
Results from biogeographical and ecological studies are difficult
for nature conservation. First, range sizes of many species are much
smaller than previously conceived. Species with small range sizes are
much more vulnerable to external disturbances than broadly dis-
tributed species and even local perturbations can lead to biodiversity
loss (Bland & Collen, 2016; Delic, Trontelj, et al., 2017). Second,
ignoring the vulnerability of cryptic species to multiple stressors can
underestimate threats to local populations and ultimately biodiver-
sity. Niche models forecasting the future of aquatic cryptic species,
for example, indicate that global climate change will cause the loss
of species along with genetic diversity throughout Europe (Balint
et al., 2011). There is an urgent need for assessing cryptic diversity
to reduce the potential loss from environmental change. One step in
this direction may be predictive phylogeographies. These use envi-
ronmental data and known phylogeographies of co-distributed taxa
to predict the presence of cryptic species in other taxa in the same
biome (Espındola et al., 2016). In conjunction with molecular opera-
tional units (discussed below), these rapid assessments of cryptic
diversity can assist towards improving policies and decision making
in conservation.
5.2 | Molecular operational taxonomic units
Cryptic species are de facto taken into consideration by an increas-
ing number of biodiversity studies that use sequence clusters rather
than nominal species as units for taxonomic diversity (Ryberg, 2015).
Such clusters, referred to as molecular operational taxonomic units
(OTUs, also referred as MOTUs), are delimited using methods pre-
sented in Section 2. In the amphipod literature, OTUs were used to
explore determinants of diversification rates (Hou, Sket, Fi
ser, & Li,
ski, & Grabowski, 2016; Yang et al.,
2011; Mamos, Wattier, Burzyn
2013), the geographic origin of European groundwater fauna
(McInerney et al., 2014), and species diversity–environment relation-
ships of local assemblages (Knox et al., 2012). Importantly, failing to
account for cryptic diversity in these studies is equivalent to omit-
ting known species, thereby underestimating diversification rates,
incorrectly reconstructing ancestral ranges and undervaluing local
diversity (Morvan et al., 2013; Pyron & Burbrink, 2013). Inferences
about eco-evolutionary processes and patterns drawn from OTUs
are free from biases due to morphological crypsis, although still
being dependent on the accuracy of molecular delimitation methods.
The use of OTUs in diversity analyses can be viewed as a logical
extension of de Queiroz’s (1999) view that each biologist can select
species properties that are most relevant to the question being
addressed. OTUs cannot be extended across all fields of biodiversity
science with similar success, although they may become mandatory
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FISER ET AL. | 625

BOX 2 Co-occurrence of cryptic species

Knowlton (1993) suggested that sympatry and local co-occurrence is common among cryptic species in the sea. Recent studies from
many animal phyla largely support this view; no less than 20% of the cryptic amphipod species were found to live in sympatry or
even syntopy.
Assuming that cryptic species significantly overlap in their ecological niche space, niche differentiation cannot explain their coexis-
tence (Chesson, 2000). Several studies addressed this issue using various model organisms, including rotifers (Montero-Pau, Ramos-
 mez, 2011; Montero-Pau & Serra, 2011; Ortells, Gomez, & Serra, 2003), nematodes (De Meester, Derycke,
Rodrıguez, Serra, & Go
Bonte, & Moens, 2011; De Meester et al., 2016; Derycke et al., 2008), different amphipods (Cothran, Henderson, et al., 2013;
Cothran, Noyes, & Relyea, 2015; Cothran, Stiff, Chapman, Wellborn, & Relyea, 2013; Dionne, Vergilino, Dufresne, Charles, & Nozais,
2011; Eisenring et al., 2016; Fi
ser et al., 2015; Wellborn & Cothran, 2004), chironomids (Pfenninger & Nowak, 2008), bugs (Saleh,
Laarif, Clouet, & Gauthier, 2012), bumble bees (Scriven, Whitehorn, Goulson, & Tinsley, 2016), fig wasps (Zhang, Lin, & Hanski, 2004)
and bats (Ashrafi, Beck, Rutishauser, Arlettaz, & Bontadina, 2011; Nicholls & Racey, 2006; Rutishauser, Bontadina, Braunisch, Ashrafi,
& Arlettaz, 2012). These studies unveiled emerging commonalities in co-occurrence patterns and unsolved issues with important
implications for nature conservation.
With little exception, studies showed that co-occurring cryptic species are ecologically differentiated. The degree of species differ-
entiation varies from case to case. One study showed strong differential preferences for foraging habitat (Nicholls & Racey, 2006),
whereas other cases found differences are more subtle (Fi
ser et al., 2015; Wellborn & Cothran, 2004). Co-occurrence is based on dif-
ferent trade-offs; i.e., (i) when species disperse along environmental gradients and locally outcompete each other (Eisenring et al.,
2016; Fi
ser et al., 2015; Pfenninger & Nowak, 2008; Rutishauser et al., 2012), (ii) when temporal fluctuations in environmental factors
alter competitive strength of co-occurring species over daily, seasonal or annual scales (Montero-Pau & Serra, 2011; Montero-Pau
et al., 2011; Ortells et al., 2003), (iii) where selective predation regulates the strength of the stronger competitor (Wellborn &
Cothran, 2004, 2007), and (iv) when, under various scenarios, heterospecific breeding interference favours population growth when
species is rare (Ruokolainen & Hanski, 2016; Zhang et al., 2004).
This review brought up a general issue; that is, whether and how statistically significant differences in biological traits can be
translated into ecologically meaningful differences. Some authors attempted to solve the puzzle by testing whether species co-occur-
rences are random or nonrandomly more frequent/rare with respect to distributional data (Fi
ser et al., 2015; Pfenninger & Nowak,
2008; Rutishauser et al., 2012; Saleh et al., 2012). The best evidence for coexistence was a demonstration that a species’ population
can grow if initially present in the system at low abundance (Siepielski & McPeek, 2010). This test requires laboratory controlled
experiments that are, in the case of cryptic species, quite demanding. We are aware of only two model systems that tested for coex-
istence under laboratory conditions. In the amphipod Hyalella, none of the three co-occurring species showed positive population
growth when they were introduced at low abundance in experimental mesocosms (Cothran et al., 2015). In contrast, interactions
among species of the nematode Pelloditis marina either facilitated or suppressed population growth (De Meester et al., 2011). An
ambiguous relationship between the degree of species differentiation and population growth in a community has important implica-
tions for many questions; for example, can we predict species responses to environmental change (Sinclair et al., 2016). This question
extends beyond the issue of co-occurring cryptic species. For example, if local factors mediate long-term co-occurrence of species
which outcompete each other in mesocosms, it can be expected that altered environmental conditions may reshape ecological space
and intensify competitive interactions between initially noncompeting species (Lortie & Callaway, 2006; Poisot, Canard, Mouillot,
Mouquet, & Gravel, 2012).

in ecology in the near future (Gill et al., 2016). Neglecting cryptic
species can bias inferences derived from large-scale patterns of phy-
logenetic diversity and phylogenetic turnover, especially when the
proportion of convergently evolved cryptic species is high (Fritz &
Rahbek, 2012; Safi et al., 2011). However, applying this approach to
conservation biology (Asmyhr, Linke, Hose, & Nipperess, 2014) and
local community ecology (Elbrecht & Leese, 2015; Jones, Ghoorah, &
Blaxter, 2011) can be risky. OTUs of unknown vulnerability to differ-
ent threats lack protection, and their ecological role in local assem-
blages cannot be inferred from phylogenetic relatedness alone (Best,
Caulk, & Stachowicz, 2013; Best & Stachowicz, 2013, 2014; Kembel,
2009).
5.3 | Making use of different species criteria
Using OTUs and treating cryptic species as a source of accountable
bias are complementary approaches for integrating cryptic diversity
into biodiversity science. However, neither satisfactorily integrates
the various properties of speciation towards a better understanding
of biodiversity patterns. We now discuss how a broader use of
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|ET AL.
FISER


626



FISER ET AL.
F I G U R E 6 A general methodology for integrating multiple species criteria into the analysis of large-scale biodiversity patterns. Individuals
can be assigned to different species hypotheses according to different criteria. Alternative data sets can be mapped in space, and regions
where different speciation mechanisms operate can be pinpointed and tested for causal environmental factors using multimodel inferences and
variance partitioning. PTP, Poisson tree processes models; GMYC, generalized mixed Yule-coalescent approaches; BP&P, Bayesian
phylogenetics & phylogeography; AICc, Akaike’s information criterion corrected for small sample size
species properties in testing eco-evolutionary hypotheses can foster
our understanding of large-scale biodiversity patterns.
The regional number of species is ultimately determined by three
processes—speciation, extinction and dispersal (Wiens, 2011). Fur-
ther, the contribution of speciation to species richness and the rela-
tive importance of different speciation properties can vary across
geographic regions and in time (Jablonski, Roy, & Valentine, 2006).
Thus, geographic variation in the proportion of morphologically cryp-
tic (OTUs) and morphologically distinguishable species could pinpoint
(hypothesis driven) how environmental factors contribute to species
richness patterns via variation in species properties during specia-
tion. An underlying hypothesis is that morphological and ecological
distinctness can be acquired much faster along a resource gradient
with varying selection pressures (ecological speciation) than from a
physical barrier with similar selection pressures in each environment
(nonecological speciation, perhaps driven by PNC; Wiens et al.,
2010; Pyron et al., 2015). An important point here is that these
hypothesis-driven predictions can be tested by integrating different
species criteria into ecological analyses (Figure 6).
One step towards this testing consists of building occurrence
databases in which thousands of specimens collected across large
geographic regions can be associated with multiple species hypothe-
ses based on morphology and multiple DNA-based criteria (Figure 6).
Note that species hypotheses can be refined as more data and
methods become available (e.g., new genes, ecological data). Ulti-
mately, one can assess the relative importance of different mecha-
nisms explaining species richness patterns for the different species
hypotheses. In our example (Figure 6), the relative importance of
spatial heterogeneity, present climate/productivity and historical cli-
mate variability for explaining biodiversity patterns is assessed using
multimodel inferences and variance partitioning (see, e.g., Eme et al.,
2015, 2017). For illustration, DNA-based criteria increase the pro-
portion of geographic variation in species richness attributed to spa-
tial heterogeneity due to the disproportionately higher number of
allopatric cryptic species in highly fragmented regions. In fact, this
approach can contribute towards understanding how mechanisms
causing cryptic diversity vary in strength relative to each other
across taxa and geographic regions.
Hey et al. (2003) used the term “species uncertainty” to denote
the ambiguous correspondence between a taxon delimited using any
criteria and the evolving entity for which it is used in a hypothesis.
The authors argued that “this scientific uncertainty cannot be
“solved” or stamped out, but neither need it be ignored or feared.”
Recent progress made in conceptualizing and delimiting species
notably opens the door for broader consideration of this uncertainty
in hypothesis testing of eco-evolutionary theories in biodiversity
science.
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| 627
6 | CONCLUSIONS
(1). Cryptic species refer to a heterogeneous and negatively defined
set of species lacking morphological distinguishability. Evolution-
ary mechanisms leading to morphological similarity are hetero-
geneous, comprising recent divergence, niche conservatism and
morphological convergence. They are as important and fascinat-
ing as mechanisms leading organisms to diversify into a multi-
tude of phenotypes. We are only just beginning to understand
the “invisible” world of cryptic species. We now need explicit
testing of whether morphological traits evolve neutrally, are
constrained by stabilizing selection, or converge from distantly
related lineages in response to similar directional selection on
morphology. At present, the relative importance of different
explanations of cryptic diversity remains largely unknown.
(2). Taxonomy can provide evidence for evolutionary explanations
if research efforts are oriented towards species hypotheses
that are theoretically and empirically grounded in the specia-
tion process. DNA taxonomy provides an ever-increasing vari-
ety of methods for delimiting cryptic species, and be used to
explore species boundaries related to morphology, ecology
and physiology. Comprehensive analyses of multiple types of
data can unveil generalities in the speciation process,
improve our understanding of the heterogeneity (species
properties) in speciation and allow better integration in biodi-
versity science.
(3). Cryptic species are often considered in biodiversity research as
evidence of incomplete species inventory or as potential
sources of bias. Paradoxically, the majority of known cryptic
species are undescribed or un-named and thus overlooked in
research fields relying on species binomials. Studies in evolu-
tion and ecology increasingly use molecular operational taxo-
nomic units (OTUs), thereby inherently incorporating cryptic
species into their analyses, but no study to date has used mul-
tiple criteria for species delineation. Extending multicriteria
approaches to different fields of biodiversity science can better
integrate cryptic species in ecological and evolutionary theo-
ries, paving the way to new frontiers in biodiversity science.
For example, are biodiversity patterns inferred from morpho-
logically and DNA delimited species discordant? If so, is dis-
crepancy a contingency to ecological and evolutionary
processes generating cryptic species? How do different mecha-
nisms causing cryptic diversity vary in strength relative to each
other across geographic space, and environmental gradients?
And lastly, do coexistence mechanisms at local scales change
as lineage divergence proceeds?

628 | FISER
(4). The phenomena of cryptic and ecological species can be parallel.
Importantly, cryptic species clearly complement research on spe-
ciation. We do envision that with the development of new
methodologies, cryptic species pervasiveness within the broader
context of biodiversity science will likely fade over time and be
viewed by the next generation of scientists as a constructive
epiphenomenon towards integrating speciation and its hetero-
geneity (species properties) into biodiversity science. This inte-
gration necessarily must include integrative taxonomy and the
use of multiple species criteria, as already evident in basic biodi-
versity research. Importantly, shifts to integrative taxonomy and
multicriteria have profound implications in terms of forecasting
and consolidating new skills and occupations in biodiversity
assessment and conservation. In the future, conservationists
and policymakers must be prepared to make informed decisions
using a more complex but novel body of knowledge on species
diversity and distribution. For example, this information may
include continental maps of species richness and geographic
range size using different species delimitation methods that can
pinpoint regions in method incongruences. These incongruences
then will reveal geographic variation in the speciation process.
Thus, better understanding of the causes of this variation in
speciation can reinforce process-oriented conservation strate-
gies. Lastly, incongruences that cannot be readily explained can
promote the development of adaptive conservation principles
and public policies that explicitly acknowledge the scientific
uncertainty of species entities.
ACKNOWLEDGEMENTS
This study was funded by the PHC Proteus programme (no.
31199UM), the Slovenian Research Agency (ARRS, Programme P0-
0184) and the Swiss National Science Foundation (grant
€ rz analysed data from Amphipoda
IZK0Z3_169642). Anne-Nina Lo
Newsletters. We thank F. Altermatt, T Datry, C Douady, D. Eme,
J.-F. Flot, L. Bernatchez and two anonymous reviewers for comments
on early version of the manuscript. This article is based upon work
from COST Action DNAqua-Net (CA15219), supported by the COST
(European Cooperation in Science and Technology) programme.
CONFLICT OF INTERESTS
The authors declare no conflict of interest.
AUTHOR CONTRIBUTION
C.F. gathered the literature data, and all authors contributed original
ideas and helped draft the paper.
ORCID
Cene Fiser http://orcid.org/0000-0003-1982-8724
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