Received: 19 January 2021 Revised: 11 February 2021 Accepted: 16 February 2021
PROBLEMS AND PARADIGMS
Prospects & Overviews
How to become a crab: Phenotypic constraints on a recurring
Joanna M. Wolfe1Javier Luque1,2,3 Heather D. Bracken-Grissom4
1Museum of Comparative Zoology and
Department of Organismic & Evolutionary
Biology, Harvard University, Cambridge,
2Smithsonian Tropical Research Institute,
3Department of Earth and Planetary Sciences,
Yale University, New Haven,Connecticut, USA
4Institute of Environment and Department of
Biological Sciences, Florida International
University, North Miami, Florida, USA
Joanna M. Wolfe, Museum of Comparative
Zoology and Department of Organismic &
Evolutionary Biology,Harvard University, 26
Oxford St, Cambridge, MA 02138, USA.
Natural Sciences and Engineering Research
Council of Canada, Grant/AwardNumber:
Postdoctoral Fellowship;National Science
Foundation, Grant/Award Numbers: 1856667,
A fundamental question in biology is whether phenotypes can be predicted by ecologi-
cal or genomic rules. At least five cases of convergent evolution of the crab-like body
plan (with a wide and flattened shape, and a bent abdomen) are known in decapod
crustaceans, and have, for over 140 years, been known as “carcinization.” The repeated
loss of this body plan has been identified as “decarcinization.” In reviewing the field,
we offer phylogenetic strategies to include poorly known groups, and direct evidence
from fossils, that will resolve the history of crab evolution and the degree of pheno-
typic variation within crabs. Proposed ecological advantages of the crab body are sum-
marized into a hypothesis of phenotypic integration suggesting correlated evolution of
the carapace shape and abdomen. Our premise provides fertile ground for future stud-
ies of the genomic and developmental basis, and the predictability, of the crab-like body
Anomura, Brachyura, carcinization, convergent evolution, Crustacea, morphological integration,
Biologists strive to explain the evolution of form, and the drivers of
biodiversity across related groups. Instances of convergent evolution
are emerging model systems to link such evolutionary patterns and
processes, as they provide naturally occurring experimental replicates,
including evidence of shared phenotypic constraints. Here, we focus on
the success of the crab body plan within the economically and ecologi-
cally significant decapod crustaceans, as a system to address these fun-
Crabs are one of the most iconic groups of invertebrates,as they play
an integral role in the aquarium trade, fisheries and aquaculture, and
are celebrated through festivals, parades, and social media memes, and
as the constellation and astrological sign Cancer. The groups we refer to
as crabs are members of two decapod crustacean infraorders, together
known as Meiura. These comprise Brachyura or “true” crabs (e.g., fid-
dler crabs, spider and decorator crabs, mud crabs,frog crabs, and swim-
ming crabs), and Anomura or “false” crabs (e.g., porcelain crabs, hermit
and king crabs, mole crabs, and squat lobsters). The most visible differ-
ence between true and false crabs is the apparent difference in num-
ber of walking legs: four and three pairs, respectively (the posterior pair
is present but reduced in anomurans, often concealed in the gill cham-
ber). Several other features differentiate anomurans and brachyurans,
such as the position of the molting plane of weakness, the length of the
antennae (usually longer in anomurans), and the position of antennae
with respect to the eyes (one pair to the side of the eyes in anomu-
rans, both pairs of antennae between the eyes in brachyurans).[1,2] The
overwhelming majority of extant decapod species (>9500 of ∼15,000)
are meiurans. By contrast, the remaining diversity of decapods is dis-
tributed into eight other infraorders and one suborder, including lob-
sters, crayfish, prawns, and shrimp.
Carcinization (a generally wide and flattened shape; Figure 1 and
Box 1), or the crab-like body plan, has evolved at least five times,
and has been lost at least seven times within meiuran crustaceans
BioEssays. 2021;2100020. © 2021 Wiley Periodicals LLC 1of14wileyonlinelibrary.com/journal/bies
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FIGURE 1 Basic anatomical terminology for an exemplar king
crab (Lithodoidea: Lithodidae: Paralithodes camtschaticus)
(simplified in Figure 2). The reasons for repeated evolution of the
crab-like body plan remain a mystery,[4,5] although there seems to
be a correlation between body form and ecology, with protective
and locomotory behaviors as examples. Carcinized lineages thrive in
almost every habitat on Earth, ranging from lively coral reefs to iso-
lated marine caves, from abyssal oceanic plains to mountain streams,
from terrestrial to aquatic ecosystems. Morphological disparity across
carcinzed lineages is equally impressive, with body shapes in endless
forms most beautiful, and sizes ranging from millimeters to meters.
Given the high morphological variation, species richness, and broad dis-
tribution of extant crabs, and their rich fossil record (Figure 3), crabs
are an ideal group to study trends in biodiversity through time.
Convergence is common on relatively recent timescales (fewer
than ∼20 million years), such as in island ecomorphs in anoles and
plants, mimicry in butterflies, and microbiota composition in car-
nivorous plants, among numerous examples. Ancient events (over
540 million years ago) also result in convergence, such as the evolu-
tion of metazoan eyes. In the latter cases, the phenotype is usually not
replicated as precisely. Meiuran evolution reflects moderate dis-
tances between groups, approximately 200–350 million years. As
we do not currently know whether parallelism (deep homology, or
conservation of pre-existing ancestral genetic regulatory mechanisms)
or “true” convergence (homoplasy, or similar phenotypes arising from
completely different ancestors) underpins the crab-like body plan, we
use the general term “convergence” to refer to the pattern of repeated
evolution of carcinization. The crab system is an emerging example
where it is becoming possible to trace the pattern of convergence, infer
shared constraints on the body form, and eventually uncover underly-
ing mechanisms and new strategies to predict phenotypic evolution.
CARCINIZATION HAS BEEN GAINED AND LOST
THROUGHOUT DECAPOD EVOLUTION
Attempts to infer the convergent pattern of carcinized forms have
inspired crustacean researcher for over 140 years.[4,5,13–20] From a
hypothesis based on our previous phylogenetic contributions[2,4,11]
(Figure 2), evolution of carcinization has fully occurred once or twice
in Brachyura (>7000 species of true crabs), in sponge crabs(Figure 2A)
and especially in eubrachyurans (Figures 2E–F, 3J), and at least three
times during the evolution of Anomura (>2500 species) in porcelain
crabs (Figures 2H, 3B), hairy stone crabs (Figure 2J), and king crabs
(Figure 2N).[4,5,13 ] Carcinization has been lost at least seven times, and
likely several other times, among fossil and living meiurans, repre-
senting instances of decarcinization, or a dramatic departure from an
ancestral crab-likebody form. Note that the pattern of carcinization we
primarily describe is not the only possible path of character evolution,
but will provide a working hypothesis for the purposes of our discus-
Progress in resolving crab relationships
Most prior phylogenetic studies have focused on the evolution-
ary pathway and ancestry of king crab carcinization (Figure 2L–N),
addressing questions about the evolution “from king [crab] to hermit
[crab], or hermit to king”?[4,17,18,20–23] Despite their carcinized appear-
ance (with broad carapaces and reduced, bent pleons), king crabs are
anomurans; their affinity is immediately evident from the specialized
posteriormost walking leg. Indeed, all recent phylogenetic work sug-
gests king crabs have evolved from a paraphyletic grade of pagurid
hermit crabs (Figure 2M).[4,11,20,23,24 ] Other examples of carcinization,
such as porcelain crabs (Figures 2H, 3B) and especially true crabs (Fig-
ures 2A–F, 3H–J) have often been excluded from detailed comparative
research, though they offer similar insights into dramatic shifts in body
morphology.[25,26] Due to the narrow systematic focus of the past, the
unparsimonious history of crab body plan evolution must be reconciled.
Numerous topologies have been proposed for the relationships
among families within the infraorders Anomura and Brachyura. How-
ever, almost half of the branches on the crab tree of life remain dark,
the most comprehensive molecular studies including only ∼51% of the
total extant families and ∼2% of the total species.[4,27] Previous stud-
ies have included a maximum of nine housekeeping genes, or whole
mitogenomes, but are poorly resolved as these data are uninformative
for deep branching events.[28–30] Although Sanger sequencing data
WOLFE ET AL.3of14
Box 1. Carcinization is the evolutionary process leading to the crab-like body form
This form is perceived as a wide, flat oval or hexagonal shape, as opposed to the elongate, cylindrical shape of a lobster or mud shrimp.
A major feature of carcinization is thus the flattening and bending of the pleon (abdomen), to fit beneath the carapace. Basic anatomy
illustrated in Figure 1. Specific features common to most carcinized groups include:
∙A flattened and widened carapace (at least slightly wider than long), often with lateral margins (raised edges of the dorsal carapace)
∙Sternites (sclerotized ventral segments) fused to some degree into a single wide plate called the thoracic sternum or plastron
∙A flattened and bent “abdomen” or pleon, hidden from dorsal view, partially or completely covering the thoracic sternum
∙Loss or significant reduction of the uropods (appendages of the sixth pleonal somite, usually forming a tail fan in other decapods)
∙Fusion of pleonal ganglia, reduction of pleonal muscles (documented for representative anomurans and two species of
Decarcinization, or the secondary loss of the crab-like body form, has occurred multiple times in both Brachyura and Anomura. The
decarcinized form is more cylindrical, but has evolved from a wide oval shaped ancestor,[2,5] as opposed to the ancestrally uncarcinized
forms (that never evolved a crab-like form in the time since their common ancestor with mud shrimp). The striking similarity between
uncarcinized and decarcinized groups has led to erroneous classification of certain decarcinized brachyurans as uncarcinized anomuran
mole crabs[125 ]; compare Figures 2C and 2K). Common features of decarcinized crabs include:
∙An elongated, narrow carapace
∙A pleon that is not strongly flattened and/or bent, and is sometimes visible in dorsal view or even elongated
∙Legs with modified distal segments
There are varying degrees of carcinization and decarcinization,[2,5] so not all species can be easily labeled as “carcinized,” “uncarcinized,”
or “decarcinized.” Some examples include: the coconut crab Birgus latro (a semi-carcinized anomuran with a bent pleon but incompletely
fused sternites and no lateral margins) and other hermit crabs that have lost or reduced their domiciles; the porcelain crab Allopetrolis-
thes spinifrons (a “hypercarcinized” anomuran with a sexually dimorphic pleon, strongly resembling brachyurans); the homolodromiid and
homoloid brachyurans( whichhave characteristically carcinized pleons but lack wide carapaces and lateral margins; Figure 2B); the thumb-
nail crab Thia scutellata (a somewhat decarcinized eubrachyuran); and the gall-forming cryptochirid crabs (decarcinized brachyurans, but
with the female pleon modified as a large brood pouch).[13,14,25,125,126 ]
exist for Anomura, fossils have not been included in the complimen-
tary morphological matrix (and thus lack any robust systematic frame-
work). Improved phylogenomic data could leverage recent sequencing
of 410 exons that represented only 32 species of meiurans. These
loci obtained much stronger support at deep nodes than have previous
mitogenomic analyses.[11,29,30 ] Most anomuran nodes were strongly
supported, but contradicted previous phylogenies on the position of
mole crabs (Figure 2K) and relationships among non-paguroids. Several
squat lobster (Figures 2G, I, 3A) and hermit crab (Figures 2L–M, 3C)
lineages remain to be sampled. Deep brachyuran nodes were strongly
supported, but the relationships between families had variable sup-
port depending on the models applied, and several key taxa were not
included (such as most podotreme lineages, and freshwater brachyu-
The podotreme brachyurans (Figures 2A–D, 3E–I; with sexualopen-
ings borne on the coxa in females and males) are critical for infer-
ring the polarity and ancestry of carcinization (and decarcinization).
As of yet, molecular phylogenetics has been insufficient to resolve
the puzzle of podotremes, therefore our depiction of their extant
relationships in Figure 2 relies on morphological data. Anatomically,
these crabs lie in between Anomura and Eubrachyura, and all current
data strongly support a paraphyletic podotreme grade with brachyu-
ran affinity. Analysis of eight Sanger sequenced genes including 58
of ∼100 brachyuran families, analyses of mitogenomes,[30,32] and
a recent transcriptomic analysis each recovered podotreme para-
phyly (the former with weak support). Relationships recovered among
podotremes were entirely contradictory between those analyses. Of
11 extant podotreme families, however, over one third lack molecu-
lar data: no sequences have been published for Poupiniidae, Lyreidi-
dae, and Phyllotymolinidae, and only a single 18S sequence is avail-
able for Homolodromiidae. Meanwhile, morphological trees, including
fossils, have sampled more extensively from podotreme lineages.[2,31]
Thus, a major goal of future research should represent all meiuran
families with morphological data, and all extant families with strongly
supported phylogenomic data, for a well-resolved total evidence phy-
Novel body plans appear to have evolved in singleton
Throughout time, there have been numerous meiurans where a single
or a very few species have evolved either carcinization from uncar-
cinized ancestors, or decarcinization from carcinized ancestors. The
most significant extant “singleton” is the carcinized anomuran Lomis
hirta (Figure 2J), forming the monotypic family Lomisidae endemic to
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FIGURE 2 Gross morphology in the convergent evolution of representative true crabs (Brachyura), porcelain crabs (Porcellanidae), hairy
stone crabs (Lomisidae), and king crabs (Lithodoidea). Losses (open circles) observed in frog crabs (Raninoidea). Topology simplified from [2,4,11].
Body plan features are assumed to be present in the common ancestor of each marked lineage but may vary considerably within each group, see
Box 1 for further details. (A) Dromioidea: Dromiidae: Conchoecetes intermedius (Phan Thiết, Vietnam). (B) Homoloidea: Homolidae: Lamoha
murotoensis (Taiwan). (C) Raninoidea: Raninidae: Raninoides benedicti (Panama). (D) Cyclodorippoidea: Cymonomidae: Cymonomus cognatus
(Taiwan). (E) Eubrachyura: Heterotremata: Xanthidae: Liomera rubra (Guam). (F) Eubrachyura: Thoracotremata: Percnidae: Percnon planissimum
(Taiwan). (G) Galathoidea: Galatheidae: Galathea pilosa (Mo’orea, French Polynesia). (H) Galatheoidea: Porcellanidae: Petrolisthes lamarckii (Taiwan).
(I) Chirostyloidea: Chirostylidae: Uroptychodes grandirostris (Taiwan). (J) Lomisoidea: Lomisidae: Lomis hirta (South Australia). (K) Hippoidea:
Hippidae: Emerita portoricensis (Rio Grande do Norte, Brazil). (L) Paguroidea: Coenobitidae: Coenobita clypeatus (Belize). (M) Paguroidea: Paguridae:
Pylopaguropsis lemaitrei (Mo’orea, French Polynesia). (N) Lithodoidea: Lithodidae: Paralithodes camtschaticus (Narvik, Norway). Photo credits: (A, N)
rej Radosta; (B, D, H, I) Tin- Yam Chan; (C, E, G, K, M) Arthur Anker; (F) Ling-Kuang Tseng; (J) Michael Marmach; (L) Darryl Felder
the southern coast of Australia and Tasmania. Over 200 years ago, the
species was classified as a member of the carcinized porcelain crabs
(Figures 2H, 3B). Further morphological examination suggested mem-
bership in the carcinized king crabs (Figure 2N), however, L. hirta is now
understood as a unique extant lineage.[34,35 ] Morphological, Sanger,
and mitogenomic data currently suggest this species is related to chi-
rostyloid (Figure 2I) and aeglid squat lobsters,[4,30,36] all of which have
The most significant fossil singleton is the decarcinized brachyu-
ran Callichimaera perplexa, a single species described from the Upper
WOLFE ET AL.5of14
FIGURE 3 Comparison of fossil meiurans representing uncarcinized (A, C, D), carcinized (B, H-J), and decarcinized (E-G) body forms. (A)
Anomura: Galatheoidea: galetheoid indet. (Pliocene, Japan). (B) Galatheoidea: Porcellanidae: Petrolisthes myakkensis (holotype UF 8678, late
Pliocene, Florida, USA). (C) Paguroidea: Diogenidae: Diogenes augustinus (holotype MPZ2020/54 articulated without its shell, left lateral view, mid
Eocene, Spain). (D) Hippoidea: Albuneidae: Italialbunea lutetiana (C-225-1, Eocene, Italy). (E) Brachyura: Callichimaeroidea: Callichimaeridae:
Callichimaera perplexa (paratype MUN-STRI 27044-02b, Late Cretaceous, Colombia). (F) Palaeocorystoidea: Palaeocorystidae: Notopocorystes
stokesi (USNM F736, Early Cretaceous, England). (G) Raninoidea: Raninidae: Raninoides willapensis (C-064-1, Eocene, USA). (H) Etyoidea:
Feldmannidae: Caloxanthus americanus (NPL-62056, Late Cretaceous, USA). (I) Dakoticancroidea: Dakoticancridae: Avitelmessus grapsoideus
(187-3, Late Cretaceous, USA). (J) Eubrachyura: Heterotremata: Carpilioidea: Zanthopsidae: Harpactocarcinus punctulatus (YPM 428818, Eocene,
indet). Photo credits: (A) Takashi Ito; (B) from Luque et al. fig. 14A; (C) Fernando Ari-Ferratges; (D, G, I) Àlex Ossó; (E, F, H, J) Javier Luque
Cretaceous with a wide distribution in Colombia and the USA (Fig-
ures 3E, 5D). A possible related taxon is the fossil Retrorsichela laevis
from the Paleocene of New Zealand, which was originally described as
a squat lobster. The shape of the fifth and sixth sternites are remark-
ably similar between C. perplexa and R. laevis. The claw morphology is
also similar, though it is also seen in other un- and decarcinized taxa
such as mole crabs (Figures 2K, 3D) and frog crabs (Figures 2C, 3F–G),
respectively. Therefore, R. laevis, if it is indeed a brachyuran and
closely related to C. perplexa, could be revised as a decarcinized form
The revelation of C. perplexa teases the potential of numerous
extinct, but unpreserved, singletons. Return to an ancestral body
plan appears to violate Dollo’s Law, but such histories have been
recorded in taxa that co-opted developmental or genetic mecha-
nisms from a common ancestor (as in the simplified case of flower
pigmentation). Conversely, new fossil discoveries could refine phy-
logenetic hypotheses and clades rather than singletons describing
a more detailed sequence of evolutionary events, as in the stepwise
decarcinization of frog crabs (Figure 3F–G).
IT IS UNCLEAR WHETHER THE EARLIEST CRABS
LOOKED LIKE CRABS
Morphologies of fossils close to the divergence time and position of a
clade are instrumental to infer whether a trait is ancestrally shared or
convergent within the group. Moreover, fossils allow phylogenies to be
scaled by time for comparative analyses, and provide Earth history con-
6of14 WOLFE ET AL.
FIGURE 4 Diagnosing the affinities of early stem group crab fossils. (A) Potential positions of early fossils following the favored phylogenomic
hypothesis. Abbreviations p2, p3 refer to the second and third pereopods. Silhouettes from PhyloPic (phylopic.org), with fossils based on
recent publications.[46,48,49] (B) Artistic reconstruction of partly carcinized Eoprosopon klugi as a facultative scavenger.(C) Artistic reconstruction
of uncarcinized Platykotta akaina as a dweller of Triassic bivalve reefs. Reconstructions by Franz Anthony
text for evolutionary events.[41–43] From fossil calibrated divergence
time estimates, it does not appear that the breadth of crab body plan
disparity was achieved early in the evolution of meiurans, due to an
early molecular divergence ∼350 million years ago, followed by a lag of
100+million years prior to the respective divergences of crown group
anomurans and brachyurans.[4,11,27] Brachyurans in particular have a
rich and disparate Late Cretaceous and Cenozoic fossil record (Fig-
ure 3E–J), witnessing bouts of morphological experimentation in sev-
eral Late Cretaceous lineages. The fossil record prior to the Late Cre-
taceous is considerably more fragmentary (preserving mainly dorsal
carapaces), obscuring understanding of early anatomical disparity and
therefore the evolution of carcinized and decarcinized forms.
The form of the common ancestor of meiurans and their sister
group, the gebiid mud shrimp, may have resembled a mud shrimp itself
(a burrower with an elongated carapace and pleon). The ancestral form
is inferred from a phylogenetic grade of mud shrimp (axiids and gebiids)
relative to meiurans, which could equally indicate the mud shrimp
forms have evolved independently, however contradictory data are
absent. Direct fossil evidence of mud shrimp prior to the Cretaceous
is largely restricted to claw fragments and traces of their burrows.
Therefore, we suggest carcinized forms did not evolve in decapods
prior to the stem group of meiurans. Unfortunately, the characteristics
of the anomuran and brachyuran stem groups are still poorly under-
stood, due to the lack of reliable fossils that can be assigned to either
clade with certainty (Figure 4).
There are only three early fossil taxa with sufficiently complete
preservation to inform ancestral states. The oldest putative brachyu-
ran fossils are the Early Jurassic Eocarcinus praecursor and Eoproso-
pon klugi (Figure 4B). Both of these fossil taxa bear sub-cylindrical
carapaces, reminiscent of those in modern homolodromiid crabs
(related to the branches of Figure 2A and/or 2B; see [2,47]). Crown
group meiurans are united by a lack of chelate second and third pere-
opods (that is, second and third thoracic legs do not have articulated
claws[1,2,48 ]). In E. praecursor, the second and third pereopods are not
fully visible, but have recently been reconstructed as distally simple
based on multiple specimens. The lack of three-dimensional infor-
mation about these limbs suggests a crown group meiuran affinity of
the species, but cannot reject anomuran affinity.[48,49] Mounting evi-
WOLFE ET AL.7of14
dence from the combination of total group brachyuran characters, and
the lack of characters shared with crown group brachyuran taxa such
as dromiaceans and homolids, together suggest that E. praecursor is a
stem group brachyuran. E. klugi exhibits similar character combina-
tions, such as the carapace grooves, claws, and pleonal posture, but
it is challenging to discern details as there is only one specimen known.
Together, these early fossils suggest the common ancestor of E. prae-
cursor,E. klugi, and crown group brachyurans was not fully carcinized,
possibly with a relatively wide carapace, a partially bent pleon, and
may have lost uropods. It is possible that crab-like forms could have
appeared multiple times, and to different degrees, within brachyurans
(with Figure 2 as one hypothesis).
The oldest putative anomuran is Platykotta akaina from the Late
Triassic (Figure 4C). This lobster-looking and uncarcinized decapod
shares features in common with some anomurans, and some that con-
tradict a brachyuran affinity, but it is known from a single specimen and
the evidence is not definitive.[48,49 ] As with E. praecursor and E. klugi,
the ventral morphology is poorly preserved. The original description
reported chelate second pereopods, which creates a contradiction.
If P. akaina indeed has distal claws on the second pereopod, either a
major character defining crown group Meiura has evolved indepen-
dently, or alternatively the species may fit well outside crown group
Meiura. Phylogenetic analyses (albeit with limited outgroup sam-
pling) recovered P. akaina in either stem group anomuran or stem group
meiuran positions. Based on the information from each of the three
important stem group taxa (Figure 4A), we hypothesize an uncarcinized
ancestor for anomurans, though the ancestral state for crown group
meiurans remains uncertain.
THE ECOLOGICAL ADVANTAGES OF BECOMING A
CRAB ARE COMPLEX
The ecological breadth of crabs (living in nearly every aquatic habi-
tat on Earth) departs from the view where convergent phenotypes are
under positive selection in their particular habitats.[6,10,51 ] Scholtz
noted that carcinization, if viewed as the overall evolution of a broad,
rounded shape from a more elongated one, is known from other
arthropods such as horseshoe crabs (whose common name leads to
mistaken identity: these are chelicerates, not crustaceans). None of
the non-meiuran groups known, however, share the bent pleon. It is
likely that carcinization in meiurans provides ecological advantages
relative to uncarcinized sister taxa (e.g., mud shrimps, squat lob-
sters), allowing them to occupy new and varied niches. These may be
broadly characterized as adaptations for protection, locomotion, and
The crab body plan may aid in protection and
The feature of carcinization most frequently discussed as adaptive is
the reduced, folded pleon. In uncarcinized decapods (including squat
lobsters and hermit crabs; Figure 2G, I and Figure 2L–M, respectively),
the elongated pleon is directly used for locomotion and predator avoid-
ance, as in the behavioral caridoid escape reaction (i.e., tail-flip or back-
wards swimming).[13,52] Bending of the pleon in c arcinization precludes
the tail-flip behavior, but instead allows crabs to avoid predators by
reducing the surface area exposed to attack. Calcification–the hard-
ening of the pleonal cuticle usually observed in carcinization–further
protects the animal from predators. The carcinized and calcified king
crabs (Figures 1, 2N) evolved from within the shell-dwelling hermit
crabs (Figures 2L–M, 3C). King crabs, and some partly carcinized hermit
crabs including B. latro[14,53] (Box 1) have therefore abandoned their
protective domiciles. The reasons are unclear, but may include mov-
ing into habitats where hiding under rocks may be favored over the
additional expense of carrying the domicile,[23,54] or scenarios where
gastropod shells were not available, forcing crabs to abandon their
Carcinization may confer other advantages, such as improvements
to locomotion. The bent pleon in combination with the flattened cara-
pace allows a lower center of gravity than in uncarcinized decapods,
freeing the posterior appendages for improved function, particu-
larly the sideways walking that typifies crabs. The sideways stance pro-
vides equally fast speeds when walking in either direction, improv-
ing avoidance of forward attacking predators from merely hiding to an
agile, active behavior. However, sideways walking is not observed in
all carcinized lineages (e.g., forward-walking spider crabs and anomu-
ran king crabs; Figure 5C and Figures 2N, 5B, respectively), and some
uncarcinzed hermit crabs can walk sideways.[14,55,56] Improvements to
mobility may also be characterized by reduced uropods associated with
carcinization (Figure 2), and specialized structures related to repro-
duction and pleonal positioning.[57–60 ] Therefore,it appears that a gen-
eral posture of the pleon is the main requirement for locomotory ben-
efits of carcinization, which can be achieved through various morpho-
Decarcinization has occurred several times, despite the presumed
loss of advantages from the exposed pleon and loss of sideways walk-
ing ability. Most decarcinized groups consist of singletons (Section 2.2)
or groups with few extant species, such as the eubrachyuran family
Corystidae and the porcelain crab genera Euceramus and Porcellanella.
If all decarcinized groups were singletons or had very limited diver-
sity, it could be hypothesized that decarcinization represents an evo-
lutionary dead-end. Contradictory evidence comes from Raninoidea,
or frog crabs (Figures 2C, 3F–G), a clade with low extant diversity (48
species) but also with >200 fossil decarcinized members dating back
to the Early Cretaceous.[40,61 ] Therefore, the crab-like body plan can-
not represent an optimum for all niches, and may be subject to func-
tional trade-offs that allow the evolution (and sometimes persistence)
of decarcinization. Extant frog crabs inhabit sediments with few hid-
ing places, and have adopted a fossorial lifestyle where rapid bury-
ing may protect the animal from predation,[40,62 ] but also conceal-
ing the animal as an ambush predator itself. Perhaps the fossorial
lifestyle exchanges lateral mobility for different protective benefits or
larger body size, a trade-off that mayallow frog crabs to persist and
diversify. Future studies of functional morphology should explicitly
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FIGURE 5 The crab-like body plan is an example of phenotypic integration. (A) Approximate areas of morphospace explored by simulations of
phenotypic evolution, after [98,100]. Integrated structures (pink and violet points, representing the simulated covariance of carapace and pleon
morphology) are constrained in the direction of variance due to their correlation. Modular, or non-integrated traits, will explore more directions of
morphospace (cyan points) due to their lack of constraints. Over time, some taxa will achieve greater disparity in constrained directions (violet
points) relative to those with modular traits, because the direction of selection is the same as the direction of constraint. (B) Example of integration
between the dorsal carapace and pleon in a carcinized taxon (Lithodoidea: Lithodidae: Paralithodes camtschaticus). (C) Example of integration
facilitating evolution of an extreme phenotype in a carcinized taxon (Eubrachyura: Majoidea: Epialtidae: Oxypleurodon alisae). (D) Example of
decoupled evolution of the carapace (cyan gradient) and pleon (solid cyan) in a decarcinized taxon (Callichimaeroidea: Callichimaeridae:
compare carcinized and non-carcinized taxa and their behaviors to bet-
ter delineate benefits of the crab-like form.
Escalation of predation cannot explain early crab
A feature of carcinization, observed mainly in eubrachyurans (Fig-
ures 2E–F, 3J) and some carcinized anomurans, is the development of
laterally mobile claws. When mineralized and adapted into forms
that suit ecology, claws have been associated with the ability to crush
prey and potentially with the diversification of the predatory crab
groups. The evolution of crabs and their efficiency as shell-crushing
predators, by adaptation of their claw morphology, has been impli-
cated as a driver of an ecological arms race called the Mesozoic Marine
Revolution. During this time, fauna such as molluscs and echinoderms
evolved stronger and more heavily ornamented morphologies, possi-
bly as a response to predation by decapod crustaceans.[65,66 ] Stud-
ies of prey taxa have focused on gastropods[67,68] and their fossils as
a proxy recording defensive evolutionary trends towards the end of
the Mesozoic.[65,69 ] Fossil crab claws that appear specialized for crush-
ing hard-shelled prey (e.g., with asymmetrical claws, “molariform” pro-
trusions on the claw tips, and/or curved “teeth” on the proximal claw
that aid in peeling open shells) are first recorded from “mid” to
Late Cretaceous deposits,[71–75 ] concurrent with the divergence of
eubrachyuran groups with known heavy shell predators such as xan-
thoids (Figure 2E) and portunoids during the so-called “Cretaceous
Upon closer examination, however, the hypothesis of claw mor-
phology and predation ability on hard-shelled invertebrates as a major
influence on the evolutionary success of crabs and their carcinized
body plans is overstated. Large claws can have other functions, includ-
ing sexually selected weapons in fiddler crabs, which do not confer
prey crushing ability but are crucial for signaling and antagonistic
behaviors.[76,77 ] Therefore, some taxa bearing large, ornamented,
and mineralized claws are not predators. The functional relationship
between carcinized forms and shell-crushing is diluted by the presence
of mineralized, asymmetrical, and ornamented claws and crushing
mandibles in other decapods, such as lobsters,[5,70] and by varied
crab diets including herbivory.[70,78–80 ] Of the carcinized anomurans,
only porcelain crabs (Figures 2H, 3B) have a known Mesozoic fossil
record.[11,81 ] Although porcelain crabs and L. hirta (Figure 2J) have
broad claws, these taxa are mainly filter feeders, occasionally using
their claws to scrape algae. While some king crabs (Figures 1, 2N)
WOLFE ET AL.9of14
are indeed reported as shell-crushing predators with heavily calcified
claws,[83,84 ] they appeared ∼35 million years after the end of the
Overall, there is little relationship observed between gross claw
morphology and function, and the timing or success of carciniza-
tion. While predation represents an effective ecological strategy for
many groups of meiurans (and investigations into species of aquacul-
tural interest may corroborate predatory behaviors), it cannot be
directly related to the evolution of body form or success of those
THE CRAB BODY PLAN MAY REPRESENT A CASE
OF PHENOTYPIC INTEGRATION BETWEEN THE
PLEON AND CARAPACE
Repeated evolution of the crab body plan may entail phenotypic inte-
gration, that is, covariation among body parts (Figure 5). Integra-
tion, usually attributed to functional or developmental relationships
between the body parts, molds phenotypic evolution in various ani-
mal systems, such as correlation between the shapes of regions of
vertebrate skulls, for example,[87–89] heads and mandibles in ants,
and appendage segments in mantis shrimp. Above, we described
possible ecological benefits for pleonal reduction in crabs, improving
their ability to hide in narrow spaces and move faster. We hypothe-
size that carcinization broadly represents an example of morphologi-
cal and functional integration, wherein the bent pleon has coevolved
with the flattened and widened carapace, possibly emergent from func-
tional improvements to predator avoidance and locomotion.
Certain carcinized features may predispose the emergence of oth-
ers, such as the bent pleon necessitating reduction of pleonal mus-
cles and fused pleonal ganglia. In brachyurans, the evolution of spe-
cialized pleon holding structures correlates with carcinization,[57,59,60 ]
while king crabs (Figures 1, 2N, 5B) calcified and folded the soft asym-
metrical pleon of an ancestral hermit crab form (Figures 2L–M, 3C).
In most carcinized meiurans, the characteristic pleonal folding occurs
fairly late in development, at the transition from planktonic mega-
lopa stage to benthic juvenile forms.[19,92,93 ] Freshwater brachyu-
rans exhibit extended brood care, which lack the metamorphic transi-
tion (the time when the pleon is moved under the body) and instead
these taxa hatch immediately as relatively carcinized juveniles.[94–96 ]
For decarcinized taxa with known development, the pleon is reduced
but never folded, for example. Perhaps decarcinized or partially
carcinized taxa exhibit pedomorphosis, wherein the carapace and
pleon retain their relative positioning from larval stages (Figure 5D).
Traditionally, morphological integration has been viewed as a set
of constraints that may limit the direction and magnitude of phe-
notypic evolution, with the alternative to integration being body
parts that evolve as separate phenotypic modules that can diverge
rapidly and therefore generate disparity.[98–100 ] While the relationship
between carcinization and pleonal bending appears straightforward as
described above, this is not the case for the carapaces of meiurans as
they exhibit substantial morphological disparity. Figures 1–3 depict rel-
atively classical examples of dorsal morphology for carcinized, uncar-
cinized, and decarcinized taxa, but there are many exceptions within
phenotypic categories (Box 1) as well as “extreme” morphologies, such
as the teardrop shaped arrow crabs (the brachyuran Stenorhynchus
and the squat lobster Chirostylus, not pictured) with legs more than
twice the body length, or elbow crabs (Parthenopidae, not pictured)
with triangular carapaces and elongated claws. A preliminary study of
shape evolution has been conducted on meiuran dorsal carapaces, for
five brachyurans and one king crab, finding greater shape similar-
ity between carapaces in four of the brachyurans and the king crab,
and little between the majoid (spider or decorator crab; an example in
Figure 5C) and other brachyurans. Extremes such as the spider crabs
can break morphological expectations from both phylogeny (to resem-
ble other, related eubrachyurans) and convergence (to look like other
carcinized taxa). Therefore the crab body plan seems to contradict the
traditional wisdom that integration constrains morphological disparity.
However, a growing number of recent studies have uncovered
strong integration of body structures alongside and even facilitating
high disparity.[88,102,103] In some clades, integrated body parts may
explore fewer overall directions of morphospace than independent
structures, but they can attain a great range of shapes within those
phenotypic constraints[99,100 ] (Figure 5A–C). For crabs, it has been
proposed that divergent carapace shapes may help taxa invade new
communities or niches where local areas of morphospace are already
occupied,[104 ] perhaps promoting carapace disparity. Integrated struc-
tures may also become decoupled into modules or partial modules,
sometimes due to a change in behavior or ecology,[105,106] complicat-
ing the observed correlations in morphospace. We hypothesize such
decoupling has occurred in at least some decarcinized taxa (Figure 5D),
where the carapace and pleon may never become integrated in juve-
niles or adults. Overall, phenotypic integration is a sensible macroevo-
lutionary expression of convergent evolution,[98,106] and its pattern
should be used to quantify carcinization.
TOWARDS PREDICTING THE EVOLUTION OF
From a mechanistic perspective, phenotype is the expressed result of
genomic and transcriptomic regulation of development. Therefore, the
constraints leading to convergent evolution of carcinization may share
an underlying genomic signature. Such a proposal may seem counter-
intuitive given the morphological and functional differences between
carcinized clades; however, deep homology of development often typi-
fies the evolution of integrated structures.
It is only within the last year that high-quality genomic resources
have become available for meiurans, though only for carcinized mem-
bers. Twospecies of eubrachyuran, Portunus trituberculatus,[107,108 ] and
Scylla paramamosain[109 ] (both members of the same family), and one
species of king crab, Paralithodes platypus now have published
chromosome-level genome assemblies. The eubrachyuran Eriocheir
japonica sinensis also has a recently updated genome assembly.[111,112]
To enable comparative research on whether genomic changes have a
10 of 14 WOLFE ET AL.
relationship to the phenotypic changes defining carcinization, it will
be essential to assemble further genome sequences, particularly for
decarcinized and uncarcinized meiurans.
Currently, little is known about development of crustacean cara-
paces, or pleonal growth. Outgrowth of the dorsal carapace has
been studied in the water flea Daphnia magna and in the amphipod
Parhyale hawaiensis, both of which are hundreds of millions of years
diverged from decapods. Nonetheless, candidate genes from the gene
regulatory network patterning the fly wing were expressed in the mar-
gin of the D. magna carapace,[113 ] suggesting that the dorsal carapace
may share deep homology with proximal leg segments in other crus-
taceans, in addition to the insect wing.[114,115 ] Meanwhile, there are
few obvious candidate genes for bending of the pleon in meiurans.
Loci of interest could be identified by comparing transcriptomes across
the metamorphic transition from megalopa larva to juvenile, when the
pleon becomes folded in most crabs. One study[108 ] has implicated
decreased expression in the P. trituberculatus transcriptome at exactly
this stage for the Hox genes Ubx and abd-A (expression of the latter
patterns the pleon in P. hawaiensis[116,117] ). More is known about the
genomics of metamorphosis in lobsters[118 ] and shrimp[119 ] than in
meiurans. Therefore, it will be necessary to explore “novel” or taxon-
restricted and non-coding loci that share more sequence or expression
similarity based on degree of carcinization than on the species relation-
ships. As phylogenetic relationships among meiruans move towards
resolution (Section 2), comparative methods could be used to identify
genomic targets, for example.[120,121] Such goals come with the caveat
that convergent evolution may be predictable at some hierarchical lev-
els of biological organization, but not at others, for example.[8,122 ]
CONCLUSIONS AND OUTLOOK
Convergent gains and losses of the crab-like body plan provide an
excellent system for examining the predictability of phenotypic evo-
lution and body form over macroevolutionary timescales. Under-
standing the ecological and genomic basis underlying convergence in
body form will contribute to the importance of constraints across
the tree of life.[6,123 ] Key priorities for future investigations should
include: (1) phylogenomic sampling of poorly studied groups to better
resolve the pattern of evolution of carcinization, (2) functional mor-
phological research comparing anomurans and brachyurans to uncover
the selective benefits of carcinization, (3) morphological comparisons
interrogating the pattern of phenotypic integration and modularity
in crabs, and (4) the assembly of genomes for exemplar carcinized
and decarcinized taxa for comparative studies. Together, phylogenetic,
morphological, and genomic evidence will reveal a comprehensive evo-
lutionary scenario describing how to become a crab.
The authors thank Javier Ortega-Hernández for supporting our
research on carcinization, our colleagues who shared photos, and Franz
Anthony for collaboration on fossil reconstructions and the graphical
abstract. This work was supported by the National Science Foundation
DEB #1856679 to J.M.W., DEB #1856667 to H.D.B.-G., and a National
Sciences and Engineering Research Council of Canada (NSERC) Post-
doctoral Fellowship to J.L. This is contribution #241 from the Coast-
lines and Oceans Division in the Institute of Environment, Florida Inter-
CONFLICT OF INTEREST
The authors declare no conflict of interest.
DATA AVAILABILITY STATEMENT
Data sharing not applicable to this article.
Joanna M. Wolfe https://orcid.org/0000-0001-6708-8332
Javier Luque https://orcid.org/0000-0002-4391-5951
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How to cite this article: Wolfe, J.M., Luque, J., &
Bracken-Grissom, H.D. (2021). How to become a crab:
Phenotypic constraints on a recurring body plan. BioEssays,