The Plasticity and Developmental Potential of Termites

Abstract

Phenotypic plasticity provides organisms with the potential to adapt to their environment and can drive evolutionary innovations. Developmental plasticity is environmentally induced variation in phenotypes during development that arise from a shared genomic background. Social insects are useful models for studying the mechanisms of developmental plasticity, due to the phenotypic diversity they display in the form of castes. However, the literature has been biased toward the study of developmental plasticity in the holometabolous social insects (i.e., bees, wasps, and ants); the hemimetabolous social insects (i.e., the termites) have received less attention. Here, we review the phenotypic complexity and diversity of termites as models for studying developmental plasticity. We argue that the current terminology used to define plastic phenotypes in social insects does not capture the diversity and complexity of these hemimetabolous social insects. We suggest that terminology used to describe levels of cellular potency could be helpful in describing the many levels of phenotypic plasticity in termites. Accordingly, we propose a conceptual framework for categorizing the changes in potential of individuals to express alternative phenotypes through the developmental life stages of termites. We compile from the literature an exemplar dataset on the phenotypic potencies expressed within and between species across the phylogeny of the termites and use this to illustrate how the potencies of different life stages of different species can be described using this framework. We highlight how this conceptual framework can help exploit the rich phenotypic diversity of termites to address fundamental questions about the evolution and mechanisms of developmental plasticity. This conceptual contribution is likely to have wider relevance to the study of other hemimetabolous insects, such as aphids and gall-forming thrips, and may even prove useful for some holometabolous social insects which have high caste polyphenism.

Full text

HYPOTHESIS AND THEORY
published: 18 February 2021
doi: 10.3389/fevo.2021.552624
Frontiers in Ecology and Evolution | www.frontiersin.org 1February 2021 | Volume 9 | Article 552624
Edited by:
Heikki Helanterä,
University of Oulu, Finland
Reviewed by:
Graham J. Thompson,
Western University (Canada), Canada
Karen Meusemann,
University of Freiburg, Germany
*Correspondence:
Lewis Revely
lewis.revely@gmail.com
Seirian Sumner
s.sumner@ucl.ac.uk
Specialty section:
This article was submitted to
Social Evolution,
a section of the journal
Frontiers in Ecology and Evolution
Received: 16 April 2020
Accepted: 22 January 2021
Published: 18 February 2021
Citation:
Revely L, Sumner S and Eggleton P
(2021) The Plasticity and
Developmental Potential of Termites.
Front. Ecol. Evol. 9:552624.
doi: 10.3389/fevo.2021.552624
The Plasticity and Developmental
Potential of Termites
Lewis Revely 1,2
*, Seirian Sumner 1
*and Paul Eggleton 2
1Centre for Biodiversity and Environmental Research, Department of Genetics, Evolution and Environment, University College
London, London, United Kingdom, 2Termite Research Group, Department of Life Sciences, The Natural History Museum,
London, United Kingdom
Phenotypic plasticity provides organisms with the potential to adapt to their environment
and can drive evolutionary innovations. Developmental plasticity is environmentally
induced variation in phenotypes during development that arise from a shared genomic
background. Social insects are useful models for studying the mechanisms of
developmental plasticity, due to the phenotypic diversity they display in the form of castes.
However, the literature has been biased toward the study of developmental plasticity in
the holometabolous social insects (i.e., bees, wasps, and ants); the hemimetabolous
social insects (i.e., the termites) have received less attention. Here, we review the
phenotypic complexity and diversity of termites as models for studying developmental
plasticity. We argue that the current terminology used to define plastic phenotypes in
social insects does not capture the diversity and complexity of these hemimetabolous
social insects. We suggest that terminology used to describe levels of cellular potency
could be helpful in describing the many levels of phenotypic plasticity in termites.
Accordingly, we propose a conceptual framework for categorizing the changes in
potential of individuals to express alternative phenotypes through the developmental life
stages of termites. We compile from the literature an exemplar dataset on the phenotypic
potencies expressed within and between species across the phylogeny of the termites
and use this to illustrate how the potencies of different life stages of different species can
be described using this framework. We highlight how this conceptual framework can help
exploit the rich phenotypic diversity of termites to address fundamental questions about
the evolution and mechanisms of developmental plasticity. This conceptual contribution
is likely to have wider relevance to the study of other hemimetabolous insects, such as
aphids and gall-forming thrips, and may even prove useful for some holometabolous
social insects which have high caste polyphenism.
Keywords: social insects, Blattodea, caste differentiation, hemimetabolism, cellular biology, stem cells, Isoptera
(termites)
INTRODUCTION
Phenotypic plasticity describes how different phenotypes or forms can arise from a single
genome, and can manifest as diversity in behavior, physiology or morphology. The ability
to express such phenotypic diversity can be considered an individual’s “potency.” Phenotypic
plasticity can produce novelty, facilitating adaptation and evolution, with effects on biodiversity,
from populations to ecological communities (Whitman and Agrawal, 2009). Understanding

Revely et al. The Developmental Potential of Termites
the proximate (mechanisms by which plasticity arises) and
ultimate (effects on fitness and function) causes underpinning
phenotypic plasticity is therefore of paramount importance in
ecology and evolution (Whitman and Agrawal, 2009). Insects
are popular study subjects for phenotypic plasticity, where it
has contributed to their ecological success due to their ability
to change morphology during development, in response to
environmental cues. Such developmental plasticity produces
morphologically distinct phenotypes within a species, often
called polyphenisms (Moczek, 2010; Lo et al., 2018). Social insects
have proven a useful study group where their societies exhibit
different phenotypes in the form of reproductive “queen” and
non-reproductive “worker” castes; caste polyphenisms are well
studied in some groups (e.g., Hymenoptera), they are less well
understood in others, specifically the termites. This is surprising
as termites exhibit enormous diversity in phenotypic and levels
of potency. In this paper we discuss how the many “phenomes”
exhibited by termite castes provide us with both complexities
and opportunities to further our understanding of the nature of
plasticity and developmental potential and propose a conceptual
framework that could facilitate future research in this area.
Developmental plasticity can be described in quantitative
terms by the number of phenotypes that can be produced from
a single genome—its “potency.” Examples of this include the
distinct queen and worker phenotypes in ant and social bee and
wasp colonies; these hymenopteran species undergo complete
metamorphosis, where there is a distinct transformation from
a single pre-adult form (the larva) to an adult form (See
Box 1): only the pre-adult form can express developmental
plasticity and alter its ultimate caste fate, meaning that no
external morphological change (i.e., change occurring through
a molt) is possible once they are adults. As a result, potency of
developmental plasticity in social Hymenoptera is largely binary:
individuals are either “totipotent,” i.e., they can become any of the
caste options available to that species, or they are “committed,”
i.e., their caste fate is sealed, usually irreversibly, and they have
lost plasticity (Box 1) (Crespi and Yanega, 1995; Boomsma and
Gawne, 2018). There is of course variation within this dichotomy;
e.g., simple social species, like Polistes paper wasps, lack any form
of commitment and plasticity is retained into adulthood (Jandt
et al., 2014); caste is determined genetically in all species for
males such that even an egg is committed to a specific caste,
and this is also the case in females for a rare number of species
(Cahan et al., 2002; Julian et al., 2002; Volny and Gordon, 2002;
Cahan and Keller, 2003; Schwander et al., 2010). But largely,
in the social Hymenoptera, an individual has the potential to
become any caste until some point in development, after which it
is developmentally committed to a specific caste. It is the relative
simplicity in caste potency that has made Hymenoptera castes
popular for studies of phenotypic plasticity, and as a consequence
the concept of insect caste polyphenisms is largely considered a
dichotomy in terms of potency.
A number of social insect taxa which cannot conform to
this dichotomy are gall-forming thrips (Crespi, 1992), aphids
(Stern and Foster, 1996), and termites which are the focus of our
study. The hemimetabolous life history of species like the termites
means that they undergo incomplete metamorphosis, changing
their form gradually over multiple pre-adult molts before finally
producing a developmentally inflexible adult (Box 1). Each molt
provides an opportunity to change their level of developmental
plasticity. In other words, unlike most of the social Hymenoptera,
there is not a single switch point in termite development
during with an individual’s potency tips from completely plastic
(totipotent) to not plastic (committed). As a result, they exhibit
more complex levels of potency both within and between
species, across their phylogeny (Toubiana and Khila, 2016; Lo
et al., 2018). This difficulty in applying the mainstream binary
terminology makes it challenging to study the mechanisms and
evolutionary processes underpinning phenotypic plasticity in this
group (Corona et al., 2016; Lo et al., 2018). However, if we are able
to create a framework which allows us to utilize this complexity,
we will be able to gain a deeper understanding of these processes.
This is important as our current understanding is largely based
on mechanisms and evolution derived from holometabolous
insects; it is little known whether the same processes underpin
the more complex plasticity found in other taxa. The same can be
said of the theorized conditions surrounding major evolutionary
transitions to superorganismality, namely the need for every
colony member to be committed to a single morphologically
distinct adult caste during early development, which is largely
Hymenoptera-focused and therefore does not fully take into
account hemimetabolous modes of development (Szathmáry and
Maynard-Smith, 1995; Boomsma and Gawne, 2018). It is only
when the complexity arising from hemimetabolous systems is
incorporated into such theories that we can truly understand
the processes underpinning the evolution of higher levels of
individuality as superorganisms. A key stumbling block in
achieving this, however, is the ability to translate descriptors of
phenotypic complexity across social taxa.
Here, we provide a new conceptual framework for classifying
phenotypic diversity in termites. We explain the challenges
that termites bring to the current terminology used to describe
developmental plasticity. We apply terminology from cell biology
literature to better categorize the complexities of termite
phenotypes and discuss how these many stages of potency makes
them important for understanding developmental plasticity. We
apply these categories to examples from the termite literature
to increase the value of these hemimetabolous (eusocial)
insects for testing fundamental questions on the evolution
and mechanisms of developmental plasticity. In doing so, we
also generate a comprehensive, albeit not exhaustive, dataset
on the levels of potency found in 73 species of termites
from the literature, which allows us to highlight promising
groups for future study, using this new framework (See
Supplementary Materials 1, 2). Finally, we explore the future
research that can be generated from our study which promises
to advance our understanding on the proximate and ultimate
mechanisms of caste determination in termites, and on the
fundamental nature of phenotypic plasticity found across all
taxa. We suggest that our framework may also provide a useful
conceptual framework for understanding diverse polyphenisms
in other taxa such as aphids and gall-forming thrips (Crespi,
1992; Stern and Foster, 1996). Indeed, any rare examples within
the holometabolous social insects which don’t conform to the
dichotomous categorization will also benefit from this new more
fine-grained framework.
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Revely et al. The Developmental Potential of Termites
BOX 1 | Glossary.
Adult: The final stage after the last ecdysis. Therefore, any committed termite workers are adults, and anything not committed is as a juvenile.
Alate: Winged reproductives that undergo nuptial flights before shedding their wings and forming new colonies.
Apterous: wingless
Apterous neotenics: (Ergatoids) Neotenic reproductive that develops from a worker in higher termites or from false workers in lower termites (See Neotenic
reproductive).
Brachypterous neotenics: (Nymphoids) Neotenic reproductive that develop from nymphal instars in both lower and higher termites (see Neotenic reproductive).
They have small, non-functional, wings.
Brachypterous: reduced wings
False workers: individuals that have not diverged from the winged line and can therefore still become Nymphs, but that help the colony to a greater or lesser extent
Foraging termites: (Formally referred to as separate-piece or multiple piece nesters) Species which live in well-defined nest where workers, at some point in the
colony-cycle, will leave the nest to forage. This means the colony longevity is not limited to the availability of food. All foraging termites have true workers which can
be thought to have reduced potential. These are found in the Mastotermitidae, Hodotermitidae, most Rhinotermititdae, and all Termitidae.
Hemimetabolous: (Sensu lato) species which undergo incomplete metamorphosis due to no pupal stage. These species progress through a series of morphologically
distinct stages separated by a molt, gradually acquiring adult characteristics. Under this definition, any species with hemimetabolous (Sensu stricto) and
paurometabolous development are included.
Holometabolous: species which undergo complete metamorphosis. This involves four stages: egg, larva, pupa, and adult.
Larvae: instars which do not have externally visible wing buds and are dependent on others for survival and do not take part in work within the colony.
Molt, Progressive: The gradual development from egg via several instars into an adult. This type of molt involves an increase in body size and morphological
development. This is the default developmental program in all hemimetabolous and holometabolous insects.
Molt, Regressive: This type of molt involves a decrease in body size and/or regression of morphological development, generally with a reduction in wing bud size
in nymphal instars.
Molt, Stationary: an intermittent molt which involves no increase in body size and morphological development. This has been exhibited in several insect species
and is associated with periods of food shortage, when a larva or nymph is not capable of passing a critical mass threshold in an instar. In some termites it might be
associated with replacing worn mandibles.
Neotenic reproductive: reproductives with either no wings or small non-functional wings, that develop within a colony from any instar after L3. Gonads grow and
they develop some imaginal characters while maintaining an otherwise larval appearance; some characters, like wing pads, may regress but usually lack compound
eyes and have a less sclerotized cuticle.
Nymph: Instars with externally visible wing buds.
Presoldier: A single transitional instar during development from previous phenotype to soldier.
Pseudergates: Nymphs which have regressively molted back into a worker-like form without wing buds.
Soldier: Sterile altruistic caste which are generally morphologically and behaviorally specialized for defense.
Termite, Higher: Made up of only termite species within the family Termitidae, which only have non-flagellate gut symbionts.
Termite, Lower: All termites other than the Termitidae. They have both flagellates and non-flagellate gut symbionts.
True workers: Individuals that have diverged and are part of a separate wingless line.
Winged line: (nymphal/pterous) developmental pathway where winged phenotypes develop.
Wingless line: (apterous) developmental pathway where wingless phenotypes develop.
Wood-dwelling termites: (Formally one-piece nesters) species where a colony will live in a single piece of wood which serves as both food and nest source. Only
the winged sexuals leave the nest and when their only food source is exploited the colony will die. Species within this life type are thought to have highly flexible
development and false workers. These are found within the Termposidae, Kalotermitidae, and some species within the Rhinotermitidae.
Worker: individuals which are now independent and able to help the colony but still do not have externally visible wing buds.
THE CHALLENGES OF CLASSIFYING
DEVELOPMENTAL PLASTICITY IN
TERMITES
Originating at least 150 million years ago (Thorne et al.,
2000; Bucek et al., 2019; Evangelista et al., 2019), termites are
social cockroaches (order Blattodea), sister to the sub-social
cockroach genus, Cryptocercus (Lo et al., 2000; Inward et al.,
2007; Bourguignon et al., 2015; Bucek et al., 2019; Evangelista
et al., 2019). A traditional classification of termites is based
on symbionts: “lower termites” have bacteria and flagellates in
their guts (Figure 1C). This is true of all termite families except
the Termitidae (“higher termites”), which have no flagellates
but other gut symbionts, mostly bacteria (Figure 1C). Termites
are key cellulose decomposers in hotter ecosystems (Takamura,
2001), can feed on many substrates (grass, wood, leaf litter, or
soil) (Eggleton, 2011) and have important roles in enhancing
ecosystem resistance to drought (Ashton et al., 2019). The
value of their ecosystem services (Jouquet et al., 2011) and
the disservices they can cause to buildings and crops (Su and
Scheffrahn, 2000; Rouland-Lefèvre, 2011), makes them important
species to study (Govorushko, 2019). As a result, there is a
considerable body of literature on the natural history of termites,
providing a foundation of information on phenotypic potency
and plasticity. In this section we review the different facets of
termite life-history that provide the means to classify phenotypes
based on their level of plasticity, illustrating the difficulties of
classifying potency from current literature and highlighting the
need for new terminology to explain variation in potency.
Developmental Stage and Phenotypic
Potency
All species of termites exhibit a range of phenotypic potency
which is shared across species and largely based on their
stage in development (Miura et al., 2000; Bourguignon et al.,
2012b; Haifig and Costa-Leonardo, 2016). Phenotypic states
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Revely et al. The Developmental Potential of Termites
FIGURE 1 | Simplified developmental pathway of (A) wood nesting termites and (B) foraging termites. Solid forward arrows, progressive molts; solid backward
arrows, regressive molts; dashed arrows, potential progressive molts in some species; circular arrow, stationary molt; BN, Brachypterous neotenics. Modified after
(Korb and Hartfelder, 2008). (C) Phylogenetic relationships of termite families (cladogram) using the sister taxon Cryptoceridae as outgroup, highlighting the
phylogenetic uncertainty of life types and ambiguity surrounding which came first in evolutionary terms. Blue, Wood-dwelling termite species; Red, Foraging termite
species; Black dashed, not enough is known about this family to definitively categorize but they are likely to be wood-dwelling species, *signifies paraphyletic families.
Modified after (Korb, 2019), (See Box 1 for definitions). [photos by Bill Sands, NHM London collection:(A) Zootermopsis (B) Hospitalitermes].
exhibit plasticity along a gradient. First, high plasticity, where
an individual has the potential to become (almost) any other
phenotype, under environmental cues; e.g., first and second
instar larvae (Box 1). Second, lower levels of plasticity, where an
individual may have limited ability to change into a small number
of phenotypes; e.g., nymphs and later instar larvae. Finally, no
plasticity, where an individual is committed to a phenotypic
state and cannot change, irrespective of the environmental cue;
e.g., primary reproductives, neotenic reproductives and soldiers
(Box 1). However, there are important exceptions. Both workers
and nymphs (Box 1) show variation in their plasticity both within
and between species (Noirot, 1955; Roisin, 2000; Lainé and
Wright, 2003; Bourguignon et al., 2012b). Moreover, both egg
and larval potency can vary across species and often between
sexes (Roisin and Lenz, 1999).
In some species, phenotype is determined by sex and this
can influence phenotypic potency. This consequently makes
categorizing potency based on developmental stage purely more
difficult. For instance, high sexual size dimorphism has led to the
loss of soldier production in one sex in a number of species as well
as ancestral loss in one sex in the higher termites which have led
to the majority presence of single sex soldiers (Bourguignon et al.,
2012a). In Coptotermes lacteus, only females can become soldiers,
and so male egg and larval instars cannot become soldiers
(Roisin and Lenz, 1999). Therefore, a sex within a species may
have a lower level of phenotypic potency at all developmental
stages than the complementary sex. However, more experimental
evidence is required to determine whether the constraints on
potency of a single sex is genetically or epigenetically determined,
and if epigenetically determined, at which developmental stage
soldier production is inhibited. Consequently, defining potency
of termite phenotypes based on their developmental stage should
not be used as the only criterion.
Influence of Life-History on Phenotypic
Potency
Two main life-history types are found within termites, classified
by the relationship between foraging and nest site (Abe,
1987; Korb, 2019); these life-history types are associated with
fundamental differences in developmental plasticity. Wood-
dwelling (Box 1) species nest and feed in the same piece of
dead wood (Korb, 2019) (Figure 1A,Box 1). Species within this
life type are found throughout lower termite families (Korb
and Hartfelder, 2008; Bourguignon et al., 2015) (Figure 1C).
Wood-dwelling termites have high levels of developmental
plasticity, with progressive, regressive and stationary molts
(Box 1) allowing reversible morphological change into any
phenotype, in response to ecological and social cues (Figure 1A).
The immatures (larvae) exhibit highly plastic phenotypes and
are a stage from which all other more committed phenotypes,
for example soldiers, nymphs, primary reproductive, and
neotenic reproductive, develop. Because of this high plasticity,
and lack of commitment, working individuals of the wood-
dwelling termites are often referred to as “false workers” [See
(d), Box 1].
The second type of life-history is the foraging termites
(Abe, 1987), which have well-defined nests, but foraging takes
place away from these nests (Korb, 2019) (Figure 1B). Families
with this life-history include Mastotermitidae, Hodotermitidae,
most Rhinotermitidae, and all Termitidae (Korb and Hartfelder,
2008) (Figure 1C). Foraging termites have lower levels of
developmental plasticity than wood-dwelling species. Seasonal
cues dictate whether early instar larvae molt into winged
or wingless lines (Figure 1B,Box 1). Therefore, there is an
irreversible early commitment into either the winged line, where
winged sexuals develop from nymphal instars, or the wingless
line, which leads to “true” workers and soldiers. Consequently,
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Revely et al. The Developmental Potential of Termites
FIGURE 2 | Terminology used to describe levels of potency within cells with examples, adapted from (Kalra and Tomar, 2014), and simplified cellular developmental
pathway showing the different levels of developmental plasticity. Everything but the zygote and embryonic stem cells are cells in an adult mammal. Full arrows,
pathway from one cell type to another; dashed arrows, presence of other pathways not shown. Blue, Totipotent; Yellow, Pluripotent; Green, multipotent; Light Green,
Oligopotent (progenitor); Orange, Unipotent; Red, fully differentiated.
individuals within the wingless line are unable to become primary
winged reproductives (Figure 1B).
However, the seeming dichotomy in developmental potential
between wood-dwelling to foraging termites and “false” to “true”
workers is an underestimation of the variation in plasticity
between species. For instance, there are some species with “true”
workers that are not in fact committed to sterility and are able
to molt into wingless reproductives under particular conditions,
some species with “true” workers which can only become soldiers,
and some species with “true” workers which are at a final state.
Therefore, they exhibit differing levels of potential and should not
be defined purely as “true” workers when discussing phenotypic
potency. Instead of a purely “totipotent versus committed” view
of plasticity, we envisage a multi-level change in plasticity of
certain phenotypes between and within species. We need to
find an alternative descriptive framework that accounts for this
variation in order to facilitate a better understanding of the
complexity in plasticity across the termites.
EMPLOYING CELL BIOLOGY TERMS AS
DESCRIPTORS OF HEMIMETABOLOUS
POTENCY
There is currently no terminology sufficient to capture
the multiple levels of plasticity, and the nuances among
different categories of “committed” and “plastic” states within
hemimetabolous insects. We suggest, therefore, borrowing terms
from cell biology. Comparisons have already been made with
the mechanistic basis for aging in termites and germline cells
(Elsner et al., 2018), therefore extending this comparison to
potency may help us to better comprehend termite plasticity and
consequently hemimetabolous insects. Both hemimetabolous
insects and stem cells have potential to change into a range
of phenotypes across many periods of development, as
they are not restricted by a developmental barrier, as with
metamorphosis in holometabolous insects. This is exemplified
in the polymorphic social aphids, gall-forming thrips, and
particularly termites (Crespi, 1992; Stern and Foster, 1996). By
having a unifying framework applicable to all hemimetabolous
insects, comparisons can be made across all the levels of social
complexity; from the highly complex termites, to the subsocial
Cryptocercidae and even to solitary hemimetabolous insects like
locusts which exhibit high individual plasticity (Nalepa, 2010;
Lo et al., 2018). Here, we outline the different stem cell potency
terms, specific to mammals, and explore how they can be used
to describe termites’ and more generally hemimetabolous insect
phenotypic diversity.
Stem cells are clone-producing cells, capable of both self-
renewal and multilineage differentiation (Till and McCulloch,
1961; Metcalf and Moore, 1971). There is variation in the
capacity of different types of stem cells to differentiate into
certain mature cell lines (Weissman, 2000), with a terminology
used to describe this variation fully (Figure 2). First, Totipotent
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Revely et al. The Developmental Potential of Termites
describes a cell that can turn into any type of cell: within a
developing multicellular organism, this is the zygote, and it is
the first cell to form after fertilization (Figure 2). Pluripotent is
used to describe cells that retain the ability to renew indefinitely
and to differentiate into cells of all three germ layers (mesoderm,
endoderm, and ectoderm): these are embryonic stem cells
produced from the inner cell mass of mammalian blastocysts
(Figure 2). Pluripotent stem cells differ from totipotent cells
in that they cannot become extraembryonic cells (Evans
and Kaufman, 1981; Martin, 1981): they have lost one facet
of plasticity.
The next level of potency is multipotent cells, which
are able to differentiate into multiple organ and tissue-
specific lineages (Figure 2). These are organ- and tissue-specific
stem cells which are present eight days post-fertilization and
throughout adulthood within multicellular organisms; they
include haematopoietic stem cells (Weissman, 2000), and bone
marrow cells which can self-renew and differentiate into all
blood cell lineages (Till and McCulloch, 1961; Becker et al.,
1963; Wu et al., 1968). Multipotent cells transition through
multiple stages of irreversible maturation, before becoming
progenitor cells which cannot renew themselves. This further
loss of potency is described as oligopotent (Figure 2) (Weissman
et al., 2001). Oligopotent cells are common myeloid progenitors
or common lymphocyte progenitors (Akashi et al., 2000). They
are committed to a single lineage of a small number of mature cell
fates (Figure 2). Of these, only multipotent is needed to describe
potency levels within hemimetabolous insects.
A final level of potency in cells is termed unipotent: these are
cells that are only able to differentiate into one fully differentiated
cell type; this term is limited in use to spermatogonial stem cells,
which differentiate into sperm cells (Figure 2) (de Rooij, 2001).
The committed state is a fully differentiated cell which is are no
longer able to change into any other form; it can be considered
a mature cell and it is committed to this final state (Figure 2).
For hemimetabolous insects, it may be more appropriate and
useful to use “committed” as it better describes their development
than the more cell-centric “fully differentiated” used within stem
cell research.
CELL POTENCY TERMINOLOGY APPLIED
TO TERMITES
Here, we illustrate how cell potency terminology can be aligned
with levels of developmental plasticity in hemimetabolous
insects, particularly termites. To do this, literature data was
collated on the plasticity potential of different phenotypes within
and between termite species, across developmental stages (See
Supplementary Materials 1, 2). The developmental pathways of
73 species were identified using a Web of Science search for each
family name and development stage, refining the search by using
lower taxonomic units where necessary. Confidence in assigning
a particular level of plasticity for a given phenotype depends
on the evidence type: observational studies, using morphometric
and molting data, are less conclusive than experimental studies,
where potency has been experimentally instigated, e.g., by colony
orphaning (See Supplementary Material 2 for categorization
of the potency of each phenotype in every species and
qualitative confidence levels for each assignment). Social and
environmental pressures can limit plasticity among termite
phenotypes leaving them functionally less plastic; furthermore,
the stage in the colony cycle may influence the expression of
plasticity (Chouvenc and Su, 2014). Many of our classifications,
therefore, will require confirmatory manipulation experiments
and more data collection. Despite this, the study shows how
aligning potency terminology from the stem cell literature with
potency levels in termites provides a useful framework for
studying the evolution and mechanisms of plasticity in termites
and hemimetabolous insects generally. We now describe each
level of potency, explaining their trends across the phylogeny
and developmental stages, provide examples of differing levels
of plasticity within and between species and then highlight
exceptions to these trends that exemplify the need for a
framework that transcends the traditional metrics of plasticity
categorization (which are discussed in section “The Challenges
of Classifying Developmental Plasticity in Termites”).
Totipotent
In termites, individuals can be thought of as totipotent when
they are able to molt into all alternative phenotypes: winged
or wingless reproductives, workers or soldiers (Table 1,Box 1).
Totipotent individuals include all workers (See Figure 3A—
blue, Supplementary Materials 1, 2) and dependent larval stages
in the Termopsidae, Kalotermitidae, Serritermitidae and some
Rhinotermitidae (e.g., Prorhinotermes inopinatus, Termitogeton
planus, Psammotermes hybostoma). It also includes nymphal
stages when they are able to regressively molt back into
workers; totipotent nymphs are restricted to the lower termites
(Box 1)—the Termopsidae, Kalotermitidae and a number
of Rhinotermitidae.
Eggs, and first and second instar larvae in most species
of lower termite are totipotent; exceptions are females in
Glossotermes occulatus (Bourguignon et al., 2009), Serritermes
serrifer (Barbosa and Constantino, 2017) and Hodotermes
mossambicus (Roisin, 2000) and males in Coptotermes lacteus
(Roisin and Lenz, 1999), which cannot become soldiers
and females in Anacanthotermes ahngerianus (Roisin, 2000)
which cannot become soldiers or workers. These sex specific
developmental trajectories are more prominent in the higher
termites. Consequently, most higher termites have either only
one sex which have totipotent eggs and early instar larvae or none
at all, due to one sex not being able to produce soldiers or neither
being able to produce neotenics, respectively. For instance, in
Acanthotermes acanthothorax (Noirot, 1955), males are unable to
become soldiers and therefore eggs and the first larval instar of
males already have reduced developmental potential.
Pluripotent
Pluripotency is a small reduction in developmental potential in
comparison with totipotency, therefore they still have very high
plasticity. An example is the pluripotent workers (See Figure 3B,
Supplementary Materials 1, 2) which have diverged from the
winged line and so cannot become winged reproductives.
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Revely et al. The Developmental Potential of Termites
TABLE 1 | Applying cell potency terminology to the different developmental stages of termites; note that a single developmental stage may exhibit different levels of potency, depending on the species; furthermore, a
single level of potency can be exhibited by a range of developmental stages, across species.
Developmental stage
Potency
classification
Egg Larvae Worker Soldier Nymph Alate Primary
reproductive
Apterous
reproductive
Brachypterous
reproductive
Totipotent Can change into anything Can change into anything Can change into
anything
N/A Can regress into workers, change
into soldiers, brachypterous
neotenics and alates
N/A N/A N/A N/A
Pluripotent Can change into anything
except a soldier/worker/
Neotenic. Or can only be
Worker or PR
Can change into anything
except a soldier/worker/
Neotenic. Or can only be
Worker or PR
Can change into
soldiers and apterous
neotenics/ W and AN
but not soldiers
N/A Can change into soldiers/ workers,
alates and brachytperous neotenic.
Or worker/soldier and alate
N/A N/A N/A N/A
Multipotent Can only be primary or
brachypterous
reproductives
Can change into workers
which can become soldiers
or other worker molts/into
nymphs which can become
BN or PR
Can change into other
worker molts and
soldiers
N/A Can change into alates or
brachypterous neotenics
N/A N/A N/A N/A
Unipotent Can only become primary
reproductives
Can change into workers or
just presoldiers which
become the terminal
state/into nymphs which
can become PR
Can change into other
worker molts
Presoldiers Can only change into alates Can change
into primary
reproductives
/adultoids
N/A Preapterous
reproductives
N/A
Committed N/A N/A Terminal state Terminal
state
N/A N/A Terminal state Terminal state Terminal state
N/A is denoted when there are no instances of the particular phenotype exhibiting the potency level; BN, Brachypterous neotenics; AN, Apterous neotenics; PR, Primary reproductives; W, Workers.
However, they still have the ability to become wingless
reproductives and take over a nest when the primary queen
or king dies. Therefore, their plasticity is not so different
from totipotent workers as they are still able to span both
sterile and reproductive phenotypes. Most commonly, therefore,
pluripotency is signified by the removal of the ability to become
one particular phenotype (Table 1). This would apply also
to nymphal instars which cannot become soldiers but can
regressively molt to become a worker, therefore are able to switch
to a sterile fate (Table 1). A number of species which do not
produce neotenics will therefore have pluripotent eggs and L1,
such as the egg and L1 stages in Termes baculi (Noirot, 1955).
Furthermore, in some species one sex cannot become particular
phenotypes (e.g., soldiers); therefore they have pluripotent eggs
and L1; e.g., the males of Silvestritermes euamignathus (Haifig
and Costa-Leonardo, 2016) (Figure 3B). A less common form of
pluripotency is when an individual has lost the ability to express
two of the possible phenotypes, but the phenotypes that still can
be expressed span both sterility and reproduction. An example of
this can be seen in male workers of Silvestritermes euamignathus
(Haifig and Costa-Leonardo, 2016) (Figure 3B). Here, they can
only become sterile workers or apterous neotenics.
Examples of pluripotent workers are known throughout
both lower and higher termites, including Mastotermitidae,
Rhinotermitidae and a number of species within the Termitidae.
Pluripotent nymphal instars have only been shown within both
Reticulitermes lucifugus and Reticulitermes flavipes (Lainé and
Wright, 2003). Their nymphal instars cannot molt into soldiers
but can become every other phenotype.
Multipotent
Multipotent describes the loss of plasticity with respect to a
specific developmental pathway i.e., wingless (non-reproductive)
or winged (reproductive) of the foraging termites (Figure 1B).
Individuals still show plasticity and can molt into another
form within the pathway, but they are committed to either
a reproductive or non-reproductive pathway. For example,
nymphs of foraging termites are multipotent as they can molt
into winged alates, which are committed to dispersing, or
brachypterous neotenics, which are committed to non-dispersal;
but they are distinct from pluripotent or totipotent nymphs
as they cannot regress back into workers or soldiers: they are
committed to a reproductive fate (Table 1). Workers, and the
larvae that produce these workers, are multipotent when they can
only molt into soldiers or other worker forms and are therefore
committed to a non-reproductive fate (Table 1).
Multipotent phenotypes are mainly found within the
foraging termites. However, there may be more species-
specific complexities than initially apparent. For example,
Psammotermes hybostoma potentially has both totipotent and
multipotent workers, with earlier worker instars potentially
becoming apterous neotenics, nymphs or soldiers and the
later instars only able to become soldiers (Bourguignon et al.,
2012b) (See Figure 3C,Supplementary Materials 1, 2). Further
experimental work is required to determine the potency of these
and many other species (Table 1).
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Revely et al. The Developmental Potential of Termites
FIGURE 3 | Developmental pathways of (A) the wood-dwelling termite Hodotermopsis sjostedti, Modified after (Miura et al., 2000); (B) Females in the foraging termite
Silvestritermes euamignathus (both solid and dashed arrows) and males in the foraging termite Silvestritermes euamignathus (only solid arrows), Modified after (Haifig
and Costa-Leonardo, 2016); (C) females in the foraging termite Coptotermes lacteus, Modified after (Roisin and Lenz, 1999); (D) the foraging termite Microcerotermes
beesoni, Modified after (Rasib and Akhtar, 2012). Arrows symbolize molts. Forward arrows, progressive molts; Backward arrows, Regressive molts; dashed lines; only
one sex can molt into this phenotype. Lines symbolize morphological and physiological change without molt. L1, Larval instar 1; W1, worker instar 1; N1, nymphal
instar 1; AN, Apterous Neotenic; BN, Brachypterous Neotenic; A, alate; PS, presoldier; S, soldier; Q/K, queen/king. Blue, Totipotent; Yellow, Pluripotent; Green,
Multipotent; Orange, Unipotent; Red, Committed. (photos: A)Hodotermopsis sjostedti- https://polyphenism.wordpress.com/2006/04/01/japanese-damp-wood-
termite/hodotermopsis-sjostedti/, (B) Silvestritermes minutus—Robert Hanus,(C) Coptotermes formosanus,(D) Microcerotermes—Bill Sands, NHM
London collection.
Female eggs and early instar larvae in the foraging
termite, Anacanthotermes ahngerianus, can be considered
multipotent because they are only able to become either
primary reproductives or brachypterous neotenics (Roisin, 2000).
Therefore, females in this species exhibit severely reduced
developmental potential compared with males as they are
totipotent at the egg and early larval instar stages. When
soldier production is sex specific, it is possible that one sex
will have multipotent workers and the other sex will have
unipotent and committed workers, as seen in multipotent female
workers and committed male workers in Macrotermes natalensis
(Noirot, 1955).
Unipotent
Individuals are unipotent when they are only able to change
into one form that is similar to their current form. For example,
presoldiers, alates and pre-apterous reproductives in all species
can only become soldiers, primary reproductives and apterous
reproductives respectively. They are limited to a phenotype
within their own specific lineage and so are unipotent. Unipotent
workers are the instars preceding the final committed worker
form: they cannot molt to become soldiers (Table 1). For
instance, large worker instars L2-4 in Microcerotermes beesoni
are unipotent as they are only able to molt into other worker
forms (See Figure 3D,Supplementary Materials 1, 2) (Rasib
and Akhtar, 2012). Similarly, unipotent nymphs are those which
can only molt into alates and therefore are only able to become
winged reproductives (Table 1,Figure 3D).
Unipotent workers are mainly found in higher termites, such
as Amitermes and Microcerotermes species, and a number of
the Nasutitermitinae which have a particular sex which cannot
become a soldier. Only Coptotermes lacteus (Roisin and Lenz,
1999), Coptotermes formosanus (Chouvenc and Su, 2014), and
Hodotermes mossambicus (Roisin, 2000) in the lower termites
have unipotent workers. Unipotent nymphs can be seen in some
lower termites, which seemingly lack the ability to produce
brachypterous neotenics, but are most prevalent in the higher
termites. One instance of unipotent eggs and L1 has been
shown in Cornitermes walkeri as females only become primary
reproductives (Roisin, 1992) (Table 1).
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Revely et al. The Developmental Potential of Termites
Committed
Individuals are “committed” when they are incapable of
molting into any other form: this includes soldiers, primary
reproductives, apterous neotenics, and brachypterous neotenics.
Species where workers are the final form and cannot molt into
soldiers are also committed (Table 1); these are observed only in
a small number of species within the higher termites such as the
Macrotermitinae, and in some cases only one sex has committed
workers whilst the other sex produces multipotent workers able
to become soldiers. The Apicotermitinae are predominantly
soldierless species, and all appear to have committed workers.
However, they are poorly studied, due to the difficulty in
identification without the soldier caste (Bourguignon et al., 2016)
(See Figure 3D,Supplementary Materials 1, 2).
FUTURE DIRECTIONS
Termites show enormous phenotypic diversity due to
developmental plasticity. They therefore make excellent study
systems for fundamental questions surrounding the nature,
mechanisms and evolution of phenotypic plasticity, which are
applicable to all taxa (a, c). These questions in turn help shine
some light on longstanding questions surrounding termite
evolution (b, d). The conceptual framework we propose is made
possible through an interdisciplinary translation of terminology
from the cellular biology world into the world of termite
phenotypic plasticity. We anticipate that the formalization
of how to classify individual-level potency in termites will
facilitate further research on the proximate and ultimate bases of
termite caste evolution, and ultimately the nature of phenotypic
plasticity. We unpack a few examples here, to illustrate the utility
of our framework and to demonstrate the research potential
from identifying the parallels between cellular and termite
developmental plasticity.
Are There Conserved Mechanisms That
Characterize Changes in Potency of
Phenotypes Across Different Organisms?
Our new framework opens up opportunities to examine the
mechanistic basis for loss and gains in plasticity at a finer
scale and allows for comparisons with other taxa, such as
Hymenoptera. A phylogenetically directed comparative analysis
across termite species would reveal where and when losses and
gains in the different forms of plasticity occurred and afford the
opportunity to detect patterns of correlated environmental and
ecological traits that may explain their evolution. Much work
has been done relating the ecological context of wood-dwelling
and foraging termites which leads them to have totipotent and
more developmentally restricted workers, respectively (Korb and
Thorne, 2017; Korb, 2019). Potentially multiple losses and gains
of totipotent workers have occurred throughout the phylogeny
(Legendre et al., 2013), providing us with a good study system
to elucidate the mechanistic basis for these loss and gains.
The classifications in our framework provide the categorical
variables required for such comparative analyses to be performed.
Moreover, the lowering in potency for one sex, from multipotent
to unipotent or committed, due to their inability to become
soldiers has been observed in a number of species. These
differences have been attributed to high sexual size dimorphism
leading to the favoring of the sex which has the appropriate
size for defense of the nest (Bourguignon et al., 2012a). It has
however been shown that in some species which have low to
no sexual size dimorphism, both sex soldiers have evolved again.
Therefore, gains in potency through evolutionary time can occur
(Bourguignon et al., 2012a). This provides another avenue within
termites to explore the fundamental mechanistic basis for losses
and gains in plasticity. Furthermore, by comparing these findings
to those from Hymenopteran and cellular studies, we may be able
to find common molecular processes which have been conserved
relating to losses and gains in plasticity.
What Came First, Totipotent or the More
Developmentally Committed Workers?
By understanding the proximate mechanisms behind the changes
in developmental plasticity which arise because of varying
ecological pressures, we will be able to elucidate questions
relating specifically to termite evolution. For instance, there has
been over 30 years of debate over whether the ancestral state
of termites was a linear developmental pathway with totipotent
workers or a bifurcated pathway with more developmentally
restricted workers, with no conclusive evidence to provide an
answer (Noirot, 1985; Watson and Sewell, 1985; Legendre et al.,
2013) (Figure 1C). We see from Legendre’s (2013) phylogenetic
analyses that there have been potentially multiple emergences
of more developmentally restricted worker caste formations.
Interestingly, there has also potentially been the loss of more
developmentally restricted worker castes and the emergence
of more plastic totipotent worker species in the phylogeny.
It may be that these are examples of rapid evolution under
strong ecological pressure, whereby once foraging is required
in a species, a more developmentally restricted worker will
follow. However, the binary “totipotent or not” categorization
has inevitably hindered our ability to elucidate the ancestral
developmental state due to its coarse categorization. Instead,
by using our new framework we will be more informed on
the transitions we see across the phylogeny, be it totipotent to
pluripotent or totipotent to multipotent. The new framework will
provide greater context to what these transitions between linear
and bifurcated pathways entail and therefore break apart the
erroneous notions that all the transitions seen on the phylogeny
are the same. By bringing new light to the debate we will be
better equipped to tackle this fundamental evolutionary question
in termite biology.
What Mechanisms Underpin Different
Types of Plasticity, and Are These
Mechanisms the Same Across
Independent Evolutionary Lineages?
As we have shown, termites have high variation in potential
developmental trajectories, analogous to the developmental
potential in stem cells. Our framework benefits from the
extensive cellular literature, which defines this variation in
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Revely et al. The Developmental Potential of Termites
developmental potential. Clearly defined categories of “potency”
allow us to select precise termite phenotypes for studying
the underlying molecular mechanisms. There is already a
body of research on the molecular basis of termite plasticity,
predominantly based on the lower termites (Zhou et al., 2006;
Korb and Hartfelder, 2008; Korb, 2015), from which a suite
of molecular signatures can be identified, highlighting the
importance of juvenile hormone and its associated gene pathways
(e.g., the hexamerin genes) in caste regulation (Zhou et al.,
2006; Korb, 2015). However, research is beginning to look at
the higher termites, highlighting the importance of caste-biased
gene expression, such as for vitellogenin genes, which have
been repeatedly co-opted for diverse functions across different
castes in termites (Weil et al., 2007; Sun et al., 2019). The
new framework allows the exploration of commonalities within
potency level across phenotypes and species of termites and even
across other hemimetabolous insects like aphids, gall-forming
thrips and locusts (Crespi, 1992; Stern and Foster, 1996; Lo
et al., 2018). For instance, the soldier form is shared across
the termites and some aphids and gall-forming thrips (Tian
and Zhou, 2014). In the parthenogenetically reproductive social
aphid, Tuberaphis styraci, soldiers are determined in late first
instar female nymphs, meaning before this the female nymphs
are pluripotent, able to become either a primary reproductive
or soldier (Kutsukake et al., 2004; Shibao et al., 2010). After
the late first instar stage, individuals molt into either a soldier
which is committed or a second instar nymph which is unipotent,
before molting into a primary reproductive which is committed.
Males in this species can only become primary reproductives
so are unipotent until they molt into adults and are then
committed. It will likely also prove useful for comparing across
other taxa such as Hymenoptera, due to there being, albeit more
restricted, variation between individuals and between species
in potency level pre-metamorphosis. For example, it may be
that some exceptional hymenopteran species, like Pogonomyrmex
barbatus which have genetic caste determination and worker
polypmorphism, lose their ability to become reproductives but
retain their ability to become one of a number worker phenotypes
and therefore could be seen as multipotent at a certain stage
of development (Cahan et al., 2002; Julian et al., 2002; Volny
and Gordon, 2002; Cahan and Keller, 2003). Also, since every
male in Hymenopteran species are genetically determined to
be reproductives only, the pre-adult stages can be seen as
unipotent transitioning to committed. Moreover, a fundamental
further question is whether the molecular signatures that dictate
termite potency are the same as those molecular signatures
that dictate cell potency. The mechanisms may be conserved
across independent evolutionary events or occur via novel
mechanisms. To date, there has been very little research drawing
comparisons between termite biology and cellular biology
(Elsner et al., 2018). However, this new framework opens up
a great breadth of potential interdisciplinary research due to
identifying the amazing parallels between cellular and termite
developmental plasticity. Only by creating this framework can
we now go on to study further whether this is more than
merely analogy.
What Constitutes a Termite
Superorganism?
Termite colonies can be considered to have organism-like
characteristics (Elsner et al., 2018). Our study has identified
major conceptual parallels in development between cellular and
termite colony development, therefore, further work potentially
identifying more homologous mechanisms shared between these
will support this organism-like quality of a termite colony. This
inevitably has connections with superorganismality, leading us
to ask what characteristics a termite superorganism would have
(Boomsma and Gawne, 2018). The question of commitment
is important to any theory of phenotypic plasticity and also
for identifying candidates for superorganismality (Boomsma
and Gawne, 2018). The mainly binary development within
Hymenoptera makes it easier to establish likely candidates
for superorganismality. Research has clarified caste potentials
and therefore their relative commitment to colony roles. The
true and false worker categorization in termites are a useful
classification that do show contrasts in social complexity
probably due to changes in ecology. However, they do not
encapsulate the most important trait of workers which are
needed to be classed as superorganismal: that they are sterile
and are committed to their worker fate (Boomsma and Gawne,
2018). True workers in some species, although have irreversibly
diverged from the winged line, are still able to go on to
become apterous neotenic replacement reproductives, and
therefore have not completely committed (Noirot, 1955, 1969;
Thorne and Noirot, 1982; Roisin and Pasteels, 1987; Vieau,
1991, 1994; Watson and Abbey, 2007; Moura et al., 2011;
Haifig and Costa-Leonardo, 2016). Consequently, species with
these workers should not be classed as superorganismal as
these have not transcended to a higher level of individuality
(West et al., 2015). This current categorization used to define
whether a termite has reproductively committed workers, and
therefore is superorganismal or not, is insufficient to precisely
identify potential candidates for superoganismality. Our
new framework allows us to more accurately distinguish
between workers which are reproductively committed
(multipotent, unipotent, and committed) and those which
are not (totipotent, pluripotent). Therefore, using the most
recent definition of superorganismality (Boomsma and
Gawne, 2018), future research surrounding the transition
to superorganismality within termites should concentrate on
the transition between pluripotent and more developmentally
committed workers.
However, it seems that within termites, the prerequisite
of reproductively committed worker castes (multipotent,
unipotent, and committed workers) for superorganismality
may leave out highly socially complex species such as in the
Nasutitermitinae. Even the less socially complex species with
high plasticity have a committed soldier caste and therefore
have high inclusive fitness acting upon them. It may be that
Hymenoptera-centric definition of superorganismality will
need to be revised to allow the full extent of insect sociality
to be acknowledged. Furthermore, clearly hemimetabolous
insect development show greater parallels with cellular
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Revely et al. The Developmental Potential of Termites
development within an organism so it may be that when
revising this definition, termite sociality should be given
greater consideration.
CONCLUSION
Developmental plasticity drives the vast diversity in form
and behavior seen within and between all taxa. Research on
the patterns of phenotypic plasticity have investigated both
holometabolous and hemimetabolous insects but there is still
a bias toward the holometabolous. This bias is clear in
the work on social insects, where holometabolous research
dominates our understanding of developmental plasticity and
social evolutionary processes (Evans and Wheeler, 2001; West-
Eberhard, 2003; Toth and Rehan, 2016; Boomsma and Gawne,
2018). The existing dichotomous view of potency, derived
from social Hymenoptera, is insufficient to provide a useful
framework for termite developmental plasticity. Moreover, the
current categories for explaining potency in termites, be it
life history or developmental stage, falls short in encapsulating
the nuances of developmental plasticity, both within and
between termite species. To address this, we have highlighted
parallels in developmental potency of hemimetabolous insects
with stem cell plasticity and suggested how we might borrow
cell potency terminology to categorize potency among the
diverse phenotypes exhibited by termite species. In doing so, a
comprehensive dataset has been created on the known potencies
of phenotypes across the developmental pathways of 73 species
of termites which represent the diversity in life histories and
evolutionary relationships (See Supplementary Materials 1, 2).
We anticipate that in proposing this new terminology and
framework, that termites may become more accessible as a
resource for advancing our understanding of mechanisms and
evolution of developmental plasticity across all taxa. Future
work may discover more direct mechanistic parallels relating to
plasticity in cellular and termite development systems.
AUTHOR CONTRIBUTIONS
LR compiled the database and drafted the manuscript. LR, SS,
and PE contributed equally in editing the manuscript. All authors
contributed to conceiving the manuscript.
FUNDING
This work was supported by the Natural Environment Research
Council through the London NERC Doctoral Training
Programme scholarship to LR (Grant No. NE/L002485/1).
ACKNOWLEDGMENTS
We would like to thank Dr. Thomas Bourguignon for providing
vital material otherwise inaccessible and SS’s lab group for
constructive advice on the manuscript.
SUPPLEMENTARY MATERIAL
The Supplementary Material for this article can be found
online at: https://www.frontiersin.org/articles/10.3389/fevo.
2021.552624/full#supplementary-material
Table S1 | Termite potency descriptions.
Table S2 | Termite potency categorizations.
Table S3 | Bibliography of termite potency descriptions.
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