Complicated evolution of the caprellid (Crustacea: Malacostraca: Peracarida: Amphipoda) body plan, reacquisition or multiple losses of the thoracic limbs and pleons.

Abstract

The Caprellidea (Crustacea) have undergone an interesting morphological evolution from their ancestral gammarid-like form. Although most caprellid families have markedly reduced third and fourth pereopods (the walking thoracic limbs) and pleons (the posterior body parts), one family, Caprogammaridae, has developed pleon with swimming appendages (pleopods), whereas another family, Phtisicidae, possesses well-developed functional third and fourth pereopods. The unique character status of these families implies that there has been reacquisition or multiple losses of both pereopods and the pleon within the Caprellidea lineages. Although the Caprellidea are fascinating animals for the study of morphological evolution, the phylogenetic relationships among the Caprellidea are poorly understood. One obstacle to studying the evolution of the Caprellidea is the difficulty of collecting samples of caprogammarid species. In this study, we obtained live samples of a Caprogammaridae species and confirmed that its pleon and pleopods could perform similar locomotive functions and swimming movements as observed in gammarids. From the phylogenetic analyses on 18S ribosomal RNA gene sequences, we identified three distinct clades of Caprellidea. The ancestral state reconstruction based on the obtained phylogeny suggested that once lost, the third and fourth pereopods were regained in the Phtisicidae, while the pleon was regained in the Caprogammaridae, while we could not exclude the possibility of independent losses. In either case, the caprellid lineage underwent a quite complicated morphological evolution, and possibly the Caprellidea may be an exception to Dollo's law.

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University of Tsukuba
Title
Complicated evolution of the caprellid (Crustacea:
Malacostraca: Peracarida: Amphipoda) body plan, reacquisition
or multiple losses of the thoracic limbs and pleons
Author(s)
Ito, Atsushi; Aoki, Masakazu N.; Yahata, Kensuke; Wada,
Hiroshi
CitationDevelopment genes and evolution, 221(3): 133-140
Issue Date2011-08
Text versionauthor
URLhttp://hdl.handle.net/2241/113824
DOI10.1007/s00427-011-0365-5
Right
© Springer-Verlag 2011　
The original publication is available at www.springerlink.com

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Complicated evolution of the Caprellid (Crustacea: Malacostraca:
Peracarida: Amphipoda) bodyplan, reacquisition or multiple losses of
the thoracic limbs and pleons

Atsushi Ito1, Masakazu N. Aoki2, Kensuke Yahata1 and Hiroshi Wada1*
1Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki,
305-8572, Japan
2Shimoda Marine Research Center, University of Tsukuba, Shimoda, Shizuoka, 415-0025, Japan

Author for correspondense*: Hiroshi Wada
Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki,
305-8572, Japan
Tel & Fax: +81-29-853-4671
E-mail: hwada@biol.tsukuba.ac.jp

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Abstract

The Caprellidea (Crustacea) have undergone an interesting morphological evolution from their
ancestral gammarid-like form. Although most caprellid families have markedly reduced third and
fourth pereopods (the walking thoracic limbs) and pleons (the posterior body parts), one family,
Caprogammaridae, has developed pleon with swimming appendages (pleopods), whereas another
family, Phtisicidae, possesses well-developed functional third and fourth pereopods. The unique
character status of these families implies that there has been reacquisition or multiple losses of both
pereopods and the pleon within the Caprellidea lineages. Although the Caprellidea are fascinating
animals for the study of morphological evolution, the phylogenetic relationships among the
Caprellidea are poorly understood. One obstacle to studying the evolution of the Caprellidea is the
difficulty collecting samples of caprogammarid species. In this study, we obtained live samples of a
Caprogammaridae species, and confirmed that its pleon and pleopods could perform similar
locomotive functions and swimming movements as observed in gammarids. From the phylogenetic
analyses on 18S ribosomal RNA gene sequences, we identified three distinct clades of Caprellidea.
Ancestral state reconstruction based on the obtained phylogeny suggested that once lost, the third
and fourth pereopods were regained in the Phtisicidae, while the pleon was regained in the
Caprogammaridae, while we could not exclude the possibility of independent losses. In either case,
the caprellid lineage underwent a quite complicated morphological evolution, and possibly the
Caprellidea may be an exception to Dollo’s law.

Key words: caprellid, molecular phylogeny, 18S rRNA, pereopod, pleon, Dollo’s law

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INTRODUCTION
It is generally accepted that evolution is irreversible and that once a complex morphological
character is lost in the course of evolution, it never reappears. This concept of Dollo’s law appeals
to our statistical senses because the development of complex morphological characters requires
several steps (Gould 1970). In contrast, reduction has occurred more frequently. Thus, when
Dollo’s law is strictly applied in phylogenetic reconstruction, one has to assume that morphological
characters have undergone multiple rounds of reduction. Reduction is an important factor in
producing the morphological diversity of an organism. Among metazoans, a large number of taxa
show the reduction of several organs or tissues. An extreme example is a myxozoan, which has lost
most aspects of its multicellular bodyplan due to its parasitic lifestyle (Jimenez-Guri et al. 2007). A
crustacean of the suborder Caprellidea (Malacostraca, Peracarida, Amphipoda) also acquired a
unique bodyplan by reducing its posterior body segments and thoracic limbs.
Most of the caprellid families (Caprellidae, Caprellinoididae, Cyamidae, Pariambidae and
Protellidae) have strongly reduced third and fourth pereopods (walking thoracic limbs) and pleons
(the body part posterior to the thorax, bearing appendages that are structurally distinct from the
thoracic limbs (Schram and Koenemann 2004; Fig. 1a). The third and fourth pereopods are
completely lost or are only present in a substantially rudimentary form. The pleon is also greatly
reduced in size, not showing any segmental structure and bearing only 1 or 2 pairs of vestigial
appendages. Some morphological and molecular phylogenetic studies strongly support the idea that
the Caprellidea derived from the Gammaridea (Ito et al. 2008; Kim and Kim 1993; Myers and
Lowry 2003), which is another amphipod suborder that has well-developed third and fourth
pereopods and a pleon (Fig. 1b). Therefore, reduction of the thoracic limbs and posterior segments
occurred within the Caprellidea.
Interestingly, there are two families that do not show the above-mentioned typical
caprelid bodyplan. A family of Caprellidea, Caprogammaridae, possesses an elongated and
segmented pleon with pleopods (appendages in pleon) (Fig. 2a, b), although the third and fourth

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pereopods are rudimentary as in other caprellids (Kudrjaschov and Vassilenko 1966; Takeuchi and
Ishimaru 1991). Although three pairs of pleopods are biramous as those of gammarids (Kudrjaschov
and Vassilenko 1966; Takeuchi and Ishimaru 1991), the functional significance of the abdomen and
appendages of Caprogammaridae has been largely unknown. Members of another family,
Phtisicidae, show a distinct bodyplan. Although their pleons are strongly reduced, the Phtisicidae
possess well-developed third and fourth pereopods, which is segmented in six parts (Fig. 2c, d). The
third and fourth pereopods of the Phtisicidae function as walking limbs. Thus, the phylogeny of the
caprelids is a matter of controversy, and caprellids must have experienced complicated evolutionary
history in their morphology (Ito et al. 2008; Laubitz 1976; Laubitz 1993; Takeuchi 1993).
In order to elucidate the evolutionary history of these distinct bodyplans in caprellids, we
previously conducted a molecular phylogenetic analysis of some caprellids and gammarids using
18S ribosomal RNA gene sequence data (Ito et al. 2008). Based on these findings, we concluded
that the gammarids were likely to be paraphyletic, and thus, that the caprellid bodyplan (i.e.,
reduction of pereopods and posterior body segments) was derived from a gammarid-like bodyplan.
Although these analyses suggested that there was a phylogenetic affinity of Phtisicidae and other
caprellid families, most of the phylogenetic relationships among the caprellid families remained
unclear because some families were not included in the analysis. This was considerably problematic
due to the absence of sequence data from the Caprogammaridae. Caprogammaridae are difficult to
collect because they are only distributed in the Northwest Pacific Oceans (Takeuchi and Ishimaru
1991) and have been reported to live at approximately 100 meters below sea-level.
Recently we successfully collected some fresh samples of a caprogammarid species,
Caprogammarus gurjanovae. We reconstructed an 18S rRNA gene phylogenetic tree for the
Caprellidea, including C. gurjanovae and another bizarre caprellid family, Cyamidae, which is a
parasite on the surfaces of whales that was not included in our previous analysis. Molecular
phylogenetic analyses covering almost all caprellid families provided an important framework for
understanding the morphological transitions within Caprellidea.