- Research article
- Open Access
Remarkable convergent evolution in specialized parasitic Thecostraca (Crustacea)
© Pérez-Losada et al; licensee BioMed Central Ltd. 2009
- Received: 10 December 2008
- Accepted: 17 April 2009
- Published: 17 April 2009
The Thecostraca are arguably the most morphologically and biologically variable group within the Crustacea, including both suspension feeders (Cirripedia: Thoracica and Acrothoracica) and parasitic forms (Cirripedia: Rhizocephala, Ascothoracida and Facetotecta). Similarities between the metamorphosis found in the Facetotecta and Rhizocephala suggests a common evolutionary origin, but until now no comprehensive study has looked at the basic evolution of these thecostracan groups.
To this end, we collected DNA sequences from three nuclear genes [18S rRNA (2,305), 28S rRNA (2,402), Histone H3 (328)] and 41 larval characters in seven facetotectans, five ascothoracidans, three acrothoracicans, 25 rhizocephalans and 39 thoracicans (ingroup) and 12 Malacostraca and 10 Copepoda (outgroup). Maximum parsimony, maximum likelihood and Bayesian analyses showed the Facetotecta, Ascothoracida and Cirripedia each as monophyletic. The better resolved and highly supported DNA maximum likelihood and morphological-DNA Bayesian analysis trees depicted the main phylogenetic relationships within the Thecostraca as (Facetotecta, (Ascothoracida, (Acrothoracica, (Rhizocephala, Thoracica)))).
Our analyses indicate a convergent evolution of the very similar and highly reduced slug-shaped stages found during metamorphosis of both the Rhizocephala and the Facetotecta. This provides a remarkable case of convergent evolution and implies that the advanced endoparasitic mode of life known from the Rhizocephala and strongly indicated for the Facetotecta had no common origin. Future analyses are needed to determine whether the most recent common ancestor of the Thecostraca was free-living or some primitive form of ectoparasite.
- Maximum Parsimony
- Convergent Evolution
- Taxon Sampling
- Suspension Feeder
- Remarkable Case
The Thoracica (Cirripedia) is highly specialized in having their six pairs of thoracopods modified into a basket of cirri used in suspension feeding . In addition, their body armour consists of a system of mineralized plates. These are not shed at moults but increase gradually in size, which differs from the conventional crustacean mode of growth by a series of cuticular moults [10, 11]. Thoracican cirripedes are prime models for studies on intertidal ecology [12–15], larval settlement [16, 17], antifouling technology  and for testing theories on the evolution of life cycles and reproductive systems [3, 19–22]. The Acrothoracica (Cirripedia), though similarly suspension feeders by means of thoracic cirri, lack mineralized plates . Instead, they are symbiotic and inhabit self-excavated burrows in either corals or gastropod shells occupied by hermit crabs.
The Ascothoracida (Thecostraca) are also parasites and infest either echinoderms or cnidarians. The most plesiomorphic ascothoracids are very little modified and only the piercing mouthparts indicate their ectoparasitic mode of life. More advanced taxa, such as the Dendrogastridae, can have strongly modified endoparasitic adults with long root-like extensions of the body wall, but they always retain body segmentation and appendages . The details of host infection, including how the endoparasitic ascothoracids gain access to their host, have never been observed, but in the ectoparasitic species the adult differs little if at all from the a-cypris larva, indicating that no real metamorphosis takes place [31, 32].
The Facetotecta is the most elusive group within the Thecostraca sensu Grygier . First recorded more than 100 years ago , they occur as y-larvae in marine plankton throughout the world, but the adult stage has never been found in the wild . However, recently, Glenner et al.  induced facetotectan y-cyprids to metamorphose in vitro (Figure 2A). They moulted into a slug-shaped stage called the ypsigon, which exhibits many similarities with the rhizocephalan vermigon. From this comparison Glenner et al.  concluded that adult facetotectans are parasites and that the ypsigon initiates an internal (endoparasitic) phase of their life cycle. The similarity between the ypsigon and vermigon stages raises the question of the phylogenetic relationship between the Facetotecta and the Rhizocephala and whether their advanced modes of parasitism have a common evolutionary origin. However, a sister relationship between the Facetotecta and the Rhizocephala goes against the classic idea of a monophyletic Cirripedia, which is supported by the presence of the so-called fronto-lateral horns in the nauplii [1, 26]. The facetotectans become even more interesting by the observation that their larvae can be both abundant and diverse, such as in Okinawan waters where more than 40 putative species occur at a single study site, indicating that a similar number of undescribed parasites occur in the nearby coral reef habitat [35, 36].
Historically, the term Cirripedia was used rather loosely, often incorporating the Ascothoracida, while the facetotectan y-larvae had no systematic affiliation. Since Grygier , the subclass Thecostraca, in systematic terms, has comprised the Facetotecta (y-larvae), the Ascothoracida and the Cirripedia, while the Cirripedia consists of the Acrothoracica, the Rhizocephala and the Thoracica . Grygier  based his system on a formal numerical cladistic analysis, but having at his disposal only a limited set of morphological characters he failed to resolve relations among the three thecostracan or among the three cirripede clades. In the last 10 years, cirripede phylogeny has been studied rather intensively based on molecular datasets. It now appears that the Rhizocephala are monophyletic , as suggested by the 18S rRNA locus, and some insight has also been gained in the intrinsic relationships of the Thoracica using nuclear (18S rRNA, 28S rRNA and H3) and mitochondrial (12S rRNA and 16S rRNA) loci [39, 40]. For the Thecostraca in general, Pérez-Losada et al.  used 18S rRNA sequences to argue that the Facetotecta is the sister group to an Ascothoracida + Cirripedia clade, but this was based on only a single facetotectan species. There is accordingly an urgent need to re-examine the phylogeny of all Thecostraca using a wider taxon sampling across the five major taxa. Moreover, since Grygier , no study has presented a character matrix that covers morphological features across all Thecostraca. Such a matrix must necessarily be based on larval characters, because post-larval Facetotecta and Rhizocephala are so reduced that no features can be compared with other groups . Even a comparison between the dissimilar adults of the Ascothoracida, Acrothoracica and Thoracica meets with severe difficulties .
Here we present a large-scale analysis combining a morphological dataset of 41 larval characters with sequence data from three nuclear genes and with broad taxon sampling within all the major thecostracan groups. Our purpose was to obtain a well-supported phylogeny for testing how often parasitism evolved within the subclass and whether homology exists between the advanced metamorphosis found in both the Facetotecta and Rhizocephala. We generated a robust phylogenetic tree where the main Thecostraca relationships were depicted as (Facetotecta, (Ascothoracida, (Acrothoracica, (Rhizocephala, Thoracica)))). This topology suggests that the very similar and highly advanced mode of metamorphosis found in the Facetotecta and the Rhizocephala evolved independently, providing a remarkable case of convergent evolution into extremely specialized endoparasitism.
All our molecular and combined analyses (Figure 3) supported the Facetotecta, Ascothoracida, Acrothoracica, Rhizocephala and Thoracica as monophyletic taxa with high confidence. For the Rhizocephala, the molecular analysis by Glenner and Hebsgaard  has already provided strong support for the monophyly of this taxon, but their study did not include the Facetotecta. For the Thoracica, previous analyses had either very limited taxon sampling [46–49] or assumed the taxon to be monophyletic [39, 40]. Our analysis is therefore the first to test the monophyly of the above mentioned taxa using a comprehensive taxon sampling covering all thecostracan orders.
Morphological evidence alone could not resolve the phylogenetic position of the Facetotecta . In our ML and BMCMC analyses (Figure 3), the Facetotecta was depicted at the base of the thecostracan tree, which confirms previous results by Pérez-Losada et al.  based on a single 18S rRNA sequence from the facetotectan Hansenocaris itoi. The Facetotecta is the only crustacean taxon where the taxonomy is based exclusively on larval forms . All Facetotecta described to date belong to the genus Hansenocaris, although undoubtedly this covers a more extensive taxonomic diversity . Kolbasov et al.  provided a key to all known facetotectan species, whether formally described or not, and they list a host of morphological characters that could be used for analysing the intrinsic phylogeny of the taxon. Our molecular analysis (Figure 3) of seven facetotectans had full resolution and high support for many nodes, indicating that the gene regions used here will also be useful for resolving evolutionary relationships within the Facetotecta. This, and the many features in larval morphology, bodes well for a future phylogenetically based taxonomy of the group.
Within the Ascothoracida, our analyses did not recover a monophyletic Dendrogastridae. Similarly, Kolbasov et al.  using lattice organ morphology at a detail not coded for here, also questioned the validity of this family. Nonetheless, taxon sampling is still limited within the subclass, and it must be kept in mind that the present classification of the Ascothoracida was never claimed to be cladistically based .
Within the Rhizocephala, our ML and Bayesian trees largely agreed with the recent analysis in Glenner and Hebsgaard , although we did not retrieve a monophyletic Akentrogonida. Both the ML and Bayesian analyses confirmed previous claims that the Rhizocephala and the Thoracica are sister groups , while the Acrothoracica diverged at the base of the Cirripedia. Two evolutionary scenarios can account for this: (1), an acrothoracican-type ancestor has led equally to both the Thoracica and the Rhizocephala; (2) a thoracican-like ancestor of both lineages became modified in both the Acrothoracica and the Rhizocephala, while its morphology remains reflected in the most plesiomorphic extant thoracicans such as the Iblomorpha .
Grygier  listed a number of putative apomorphies for the Thecostraca, mostly pertaining to the presence of a cypridoid settlement stage with prehensile antennules. To his list we can now add the presence of five pairs of chemosensory lattice organs on the carapace of the cypridoid larva [50, 52–54]. These structures have not been found in any other crustaceans.
Larval characters are the only morphological traits that can be coded for all thecostracan taxa, but only Grygier  has previously presented a formalized matrix based on these features. Although our morphological dataset failed to resolve basic thecostracan radiation in the MP analysis, we did identify apomorphies in support of the monophyly of the three major groups. For the Cirripedia, one of the 11 morphological apomorphies is the classical presence of fronto-lateral horns in the nauplii, which was the first character by which the Rhizocephala could be recognized as belonging to the Cirripedia [1, 10]. The remaining 10 apomorphies all concern the cyprid, which is instrumental in enabling the complex and efficient mechanism of substratum location and attachment seen in all cirripedes irrespective of the immense differences in adult morphology and biology. As previously predicted [9, 26] these cyprid specializations, notably in the sensory and locomotory apparatus, are important in explaining the immense success of the Cirripedia compared with the other Thecostraca. When facetotectan y-cyprids and ascothoracidan a-cyprids become better analyzed at a level comparable to that of the cirripede cyprid (e.g., ), it is very likely that additional apomorphies for the Cirripedia will be revealed.
Parasitism in the Thecostraca
The Facetotecta, Ascothoracida and Rhizocephala are all parasitic and this raises the question whether parasitism in these taxa evolved independently or had some level of common ancestry. Both our outgroups contain parasitic forms, but these are all secondarily derived with high certainty. In the Malacostraca, parasites are found only in highly derived taxa such as the Amphipoda and especially the Isopoda. Both isopods and amphipods are nested deep within the Malacostraca and the parasites again deep within the two orders [56–59]. In the Copepoda all available phylogenies, notably the one by Huys and Boxshall , place the several parasitic groups well derived within the taxon. We can therefore assume a free-living ancestor at the base of both outgroups, which suggests that the ancestor of the Malacostraca, Copepoda and Thecostraca was free-living too. Making this assumption, our phylogeny indicates a shift from free-living to parasite at the base of the Thecostraca, as the Facetotecta (parasite) is the first group to branch off. However, our morphological dataset was not constructed to solve this issue, since it relies on larval characters only. Moreover, coding parasitism as a single character is a gross oversimplification, obscuring the different adaptations to this mode of life within the Thecostraca. While detailed similarities exist between Facetotecta and Rhizocephala, neither of these taxa shows any similarity to the Ascothoracida in their mode of parasitism. In the most primitive Ascothoracida there is no metamorphosis, and the adult parasite is very similar to the settling a-cypris larva. This contrasts with the profound and remarkably similar metamorphosis known from both the Facetotecta and Rhizocephala. In rhizocephalans the settled cyprid metamorphoses into a vermigon, a highly reduced stage that is injected into the haemocoelic system of the host crab and initiates the endoparasitic phase of the life cycle (Figure 2B) [29, 30, 61]. Recently, Glenner et al.  found that facetotectan y-cyprids metamorphose into a very comparable stage called the ypsigon (Figure 2A). Both the vermigon and the ypsigon are slug-shaped, unsegmented, without appendages and have an extremely simplified internal structure that includes only a handful of cell types (Figures 1 and 2). Based on these observations, Glenner et al.  concluded that the adult Facetotecta are parasitic in unknown hosts and, like the Rhizocephala, with an initial endoparasitic phase in the life cycle. Our ML and BMCMC analyses (Figure 3) found no close relation between the Facetotecta and Rhizocephala, and such a relation was rejected by both the S-H and Bayesian tests (P and pP < 0.001). If mapped onto our ML or BMCMC trees, the presence of a slug shaped, unsegmented stage (vermigon, ypsigon) appears to have evolved independently in the Facetotecta and the Rhizocephala. This remarkable convergence demonstrates the flexibility of the thecostracan body plan and the morphological diversity crustaceans can achieve when under selection for parasitism. As complementary work to the analysis presented here we would, in the future, like to include the parasitic Tantulocarida, from which we did not have material for molecular analysis [37, 62, 63]. This class of Crustacea is often assumed to be the closest relative to the Thecostraca. It would therefore be very interesting to examine if the highly advanced parasitism seen in this group is homologous to any of the several modes of parasitism found in the Thecostraca.
We conclude that the Facetotecta is a monophyletic taxon with a sister relationship to a clade consisting of the Ascothoracida and Cirripedia. Within the latter, the Acrothoracica is sister to a Rhizocephala + Thoracica clade. Facetotecta, Ascothoracida and Cirripedia are each well characterized by apomorphies in larval morphology. The very similar ypsigon and vermigon stages arose independently in the Facetotecta and the Rhizocephala and provide a remarkable case of convergent evolution. Future analyses with an enlarged morphological database and more taxa must elucidate whether the ancestors to the Thecostraca were free-living or some form of primitive ectoparasites.
We sampled 79 thecostracans including Facetotecta (seven species), Ascothoracida (five spp.), and Cirripedia (67 spp.): Acrothoracica (three spp.), Rhizocephala (25 spp.) and Thoracica (39 spp.). While there is no consensus on large-scale phylogeny of the Crustacea, the most recent and comprehensive phylogenetic analysis of arthropod relationships  based on 62 loci (41 Kb) showed that the Malacostraca is the sister clade to the Thecostraca and the Copepoda is their closest relative, confirming previous phylogenetic results by Regier et al.  and Mallat and Giribet . We, therefore, used 12 malacostracans and 10 copepods (Additional file 1, Table S1) to root the Thecostraca tree. All Facetotecta, except Hansenocaris itoi, were sampled as nauplii and reared to the y-cypris stage at the Sesoko Marine Station, Okinawa, Japan, as in Glenner et al. . DNA was extracted from samples of 10–20 y-cyprids pooled from distinct types of larvae. These types, representing still-undescribed species, were distinguished based on the morphology of moulted skins of the last nauplius V instars that developed into the y-cyprids (see ). The most recent classification of the Crustacea by Martin and Davis  lists a total of eight orders within the three thecostracan infraclasses (Facetotecta, Ascothoracida and Cirripedia), and all of these are represented in this study (see Additional file 1, Table S1; no subdivision of the infraclass Facetotecta has been attempted yet). We, therefore, think that this represents a reasonable sampling for studying basic evolutionary relationships within the Thecostraca. Specimens were preserved in 70% EtOH and are housed in the crustacean collection at the Monte L. Bean Life Science Museum, Brigham Young University.
DNA extraction, PCR and sequencing
DNA extraction, amplification, and sequencing were performed as described in Pérez-Losada et al. [39, 40]. Since this study attempts to solve the evolution of backbone lineages in the thecostracan tree, we selected the three more informative genes in Pérez-Losada et al.  for inferring deep relationships: 18S rRNA (2,305 bp), 28S rRNA (2,402 bp), and histone H3 (328 bp). As demonstrated in Pérez-Losada et al. , these genes have proven to be very informative at this level. Here we have generated 39 new sequences (18S rRNA = 13 sequences, 28S rRNA = 12, and H3 = 14), which have been deposited in GenBank under the accession numbers FJ751865–FJ751903 (Additional file 1, Table S1).
We scored a total of 41 characters in larval morphology taken from the nauplii (10), the cypridoid larvae (28) and from general development (3) (Additional file 1, Appendices S1 and S2). There is no previous morphology-based analysis of the phylogeny of the Ascothoracida or the Acrothoracica (Cirripedia), and for the Rhizocephala (Cirripedia) the morphological matrix in Høeg and Lützen  concerned only the order Akentrogonida. For the Thoracica (Cirripedia), most previously used characters were derived from the sessile adults [10, 39, 40, 42, 68], but since adult Facetotecta are unknown and adult Rhizocephala are singularly specialized for a parasitic mode of life, any morphology based matrix of all Thecostraca must be based on larval characters only. Our matrix is based on Grygier [8, 69], but we have increased the list of characters and revised definitions and scorings. Recent advances in the understanding of the ultrastructure of thecostracan larvae have yielded many new traits, especially concerning the cypridoid stage [9, 50, 53, 70–73]. On the other hand, we were compelled to omit some of the potentially important characters of Grygier . He coded the Facetotecta, Ascothoracida and Cirripedia by reconstructing their supposed ground patterns, but we used an exemplar approach, and this illustrated that accurate information on character states was lacking for many species. We therefore used '?' in all cases where the character state was unknown for a species, even if it is supposedly placed deep within a taxon with an apparently invariable morphology for the trait in question. Unexpected character states such as the occurrence of 'crest in a trough'-type lattice organs (character 13) in some Chthamalus, which are nested deep within the Thoracica, shows that this is a prudent approach.
Nucleotide sequences were aligned using MAFFT v5.7  as indicated in Pérez-Losada et al.  for each of the three thecostracan infraclasses. Final assembling of each aligned group was performed using profile alignment generating a final dataset of 6,244 sites. Uncertainty in our 18S and 28S alignments was identified using GBlocks v0.91b . No questionable regions were observed in the entire H3 alignment. GBlocks parameters (minimum number of sequences for a conserved and a flank position, maximum number of contiguous non-conserved positions, minimum length of a block and allowed gap positions) were set up as 51-85-8-10-all and 38-63-8-10-all for 18S and 28S, respectively. These settings generated a conserved alignment of 3,437 sites. Long and short (after GBlocks) aligned data sets were initially analyzed in RAxML  and almost identical ML trees were obtained. Therefore, in all the subsequent analyses performed here we used the long aligned dataset (6,244 sites). Congruence among gene regions was addressed using the Wiens  protocol. Separate bootstrap ML analyses  were conducted for each of the three genes using RAxML to detect potential areas of strongly supported incongruence as indicated by conflicting nodes with bp ≥70%. No such areas of incongruence were observed in our alignment.
Morphological and DNA sequence data were analyzed under different phylogenetic approaches. Morphological data alone were analyzed using MP as implemented in PAUP* v4b10 . We performed MP heuristic searches using 100 random addition replicates and tree bisection and reconnection branch swapping. A maxtree limit of 1,000 trees per replicate was enforced in each analysis. DNA phylogenies were inferred using the ML approach implemented in RAxML with 100 randomized MP starting trees. Morphological-DNA phylogenies were inferred using Bayesian methods coupled with Markov chain Monte Carlo (BMCMC) inference, as implemented in MrBayes v3.04b . DNA mixed model analyses were performed under both ML and BMCMC procedures. DNA model selection followed the procedure outlined by Posada and Buckley  as implemented in ModelTest v3.6 . The GTR+Γ+I model  was selected for all gene regions. Within the BMCMC approach, morphological data were analyzed using the 'standard' model. This model is based on the ideas originally presented by Lewis . Essentially, the model is analogous to a JC model  (equal substitution rates) except that it has a variable number of states (two in our case). Four independent BMCMC analyses were run in MrBayes with each consisting of four chains. Each Markov chain was started from a random tree and run for 107 cycles, sampling every 1,000th generation. Model parameters were unlinked, treated as unknown variables with uniform default priors and estimated as part of the analysis. Convergence and mixing were monitored using Tracer v1.4 . All sample points prior to reaching stationary were discarded as burn-in. The pP for individual clades obtained from separate analyses were compared for congruence and then combined and summarized on a 95% majority-rule consensus tree [87, 88].
Clade support under the MP and ML approaches was assessed using the nonparametric bootstrap procedure  with 1,000 bootstrap replicates and one random addition per replicate. Confidence in our best hypotheses of phylogenetic relationships was tested by first creating alternative hypotheses in MacClade  as indicated in Pérez-Losada et al.  and then comparing them under both likelihood and Bayesian frameworks. Likelihood topological tests were conducted using the Shimodaira and Hasegawa (S-H)  test as implemented in PAUP*. Ten thousand replicates were performed for every topology test resampling the partial likelihoods for each site (RELL model). Bayesian topological tests were performed as described in Huelsenbeck et al. .
We are very grateful to Yair Achituv and Robert Vrijenhoek and the Monterey Bay Aquarium Research Institute for specimens. This research was supported by the grants NSF DEB-0236135 to KAC and MP-L and BSF 2004-239 to KAC. JTH was financed by the Danish Natural Science Foundation (FNU), the Carlsberg Foundation, The Scandinavian Sasakawa Foundation and the European Union COBICE and SYNTHESYS programs. We are finally indebted to Henrik Glenner, Mark J. Grygier and Yoshihisa Fujita for invaluable assistance with rearing and identifying facetotectan larvae and for numerous fruitful discussions on thecostracan evolution
- Høeg JT, Møller OS: When similar beginnings leads to different ends: Constraints and diversity in cirripede larval development. Invertebr Reprod Dev. 2006, 49: 125-142.View ArticleGoogle Scholar
- Ruppert ER, Fox RS, Barnes RD: Invertebrate zoology: A functional evolutionary approach. 2003, Florence, Kentucky: Cengage LearningGoogle Scholar
- Charnov EL: Sexuality and hermaphroditism in barnacles: A natural selection approach. Barnacle biology. Edited by: Southward AJ. 1987, Rotterdam, The Netherlands: A.A. Balkema, 5: 89-103.Google Scholar
- Darwin C: A monograph of the fossil Lepadidae or, pedunculated cirripedes of Great Britain. 1851, London: Paleontological SocietyView ArticleGoogle Scholar
- Darwin C: A monograph of the sub-class Cirripedia, with figures of all the species. The Lepadidae: Or, pedunculated cirripedes. 1852, London: Ray SocietyGoogle Scholar
- Darwin C: A monograph of the sub-class Cirripedia, with figures of all the species. The Balanidae (or sessile cirripedes); the Verrucidae, etc., etc., etc. 1854, London: Ray SocietyGoogle Scholar
- Darwin C: A monograph of the fossil Balanidae and Verrucidae of Great Britain. 1855, London: Paleontological SocietyGoogle Scholar
- Grygier MJ: New records, external and internal anatomy, and systematic position of Hansen's y-larvae (Crustacea: Maxillopoda: Facetotecta). Sarsia. 1987, 72: 261-278.Google Scholar
- Høeg JT, Lagersson NC, Glenner H: The complete cypris larva and its significance in thecostracan phylogeny. Evolutionary and Developmental Biology of Crustacea. Edited by: Scholtz G. 2004, A. A. Balkema/Lisse, Abingdon, Exton (PA) & Tokyo, 15: 197-215.Google Scholar
- Anderson DT: Barnacles-structure, function, development and evolution. 1994, London: Chapman and HallGoogle Scholar
- Blomsterberg M, Glenner H, Høeg JT: Growth and molting in epibiotic pedunculated barnacles of the genus Octolasmis (Crustacea: Thecostraca: Cirripedia: Thoracica). J Morphol. 2004, 200: 154-164. 10.1002/jmor.10132.View ArticleGoogle Scholar
- Carroll ML: Barnacle population dynamics and recruitment regulation in southcentral Alaska. J Exp Mar Biol Ecol. 1996, 199: 285-302. 10.1016/0022-0981(95)00178-6.View ArticleGoogle Scholar
- Hawkins SJ, Corte-Real HBSM, Pannacciulli FG, Weber LC, Bishop JDD: Thoughts on the ecology and evolution of the intertidal biota of the Azores and other Atlantic islands. Hydrobiologia. 2000, 440: 3-17. 10.1023/A:1004118220083.View ArticleGoogle Scholar
- Miron G, Boudreau B, Bourget ETI: Intertidal barnacle distribution: a case study using multiple working hypotheses. Mar Ecol-Prog Ser. 1999, 189: 205-219. 10.3354/meps189205.View ArticleGoogle Scholar
- Chan BKK, Morritt D, Williams GA: The effect of salinity and recruitment on the distribution of Tetraclita squamosa and Tetraclita japonica (Cirripedia; Balanomorpha) in Hong Hong. Mar Biol. 2001, 138: 999-1009. 10.1007/s002270000531.View ArticleGoogle Scholar
- Clare AS: Chemical signals in barnacles: Old problems, new approaches. New frontiers in barnacle evolution. Edited by: Schram FR, Høeg JT. 1995, Rotterdam, the Netherlands: A.A. Balkema, 10: 49-67.Google Scholar
- Walker G: Larval settlement: Historical and future perspectives. New frontiers in barnacle evolution. Edited by: Schram FR, Høeg JT. 1995, Rotterdam, the Netherlands: A. A. Balkema, 10: 69-85.Google Scholar
- Aldred N, Clare AS: The adhesive strategies of cyprids and development of barnacle-resistant marine coatings. Biofouling. 2008, 24 (5): 351-363. 10.1080/08927010802256117.View ArticlePubMedGoogle Scholar
- Høeg JT: Sex and the single cirripede. New frontiers in barnacle evolution. Edited by: Schram FR, Høeg JT. 1995, Rotterdam, The Netherlands: A. A. Balkema, 10: 195-206.Google Scholar
- Buhl-Mortensen L, Høeg JT: Reproduction and larval development in three scalpellid barnacles (Scalpellum scalpellum, Ornatoscalpellum stroemii and Arcoscalpellum michelottianum, Crustacea: Cirripedia: Thoracica): Implications for reproduction and dispersal in the deep-sea. Mar Biol. 2006, 149: 829-844. 10.1007/s00227-006-0263-y.View ArticleGoogle Scholar
- Yamaguchi S, Yusa Y, Yamato S, Urano S, Takahashi S: Mating group size and evolutionarily stable pattern of sexuality in barnacles. J Theor Biol. 2008, 253 (1): 61-73. 10.1016/j.jtbi.2008.01.025.View ArticlePubMedGoogle Scholar
- Ozaki Y, Yusa Y, Yamato S, Imaoka T: Reproductive ecology of the pedunculate barnacle Scalpellum stearnsii Cirripedia: Lepadomorpha: Scalpellidae. J Mar Biol Ass U K. 2008, 88: 77-83. 10.1017/S0025315408000131.View ArticleGoogle Scholar
- Kolbasov GA, Høeg JT: External morphology of females in the burrowing barnacles Lithoglyptes mitis and L. habei (Lithoglyptidae) and the phylogenetic position of the Cirripedia Acrothoracica (Crustacea Thecostraca). Arthropoda Sel. 2000, 9: 13-27.Google Scholar
- Andersen AN: Measuring more of biodiversity: genus richness as a surrogate for species richness in Australian ant faunas. Biological Conservation. 1995, 73: 39-43. 10.1016/0006-3207(95)90059-4.View ArticleGoogle Scholar
- Høeg JT: Rhizocephala. Microscopic anatomy of invertebrates. Edited by: Harrison F. 1992, New York: Alan Liss Inc, 9: 313-345.Google Scholar
- Høeg JT: The phylogenetic position of the Rhizocephala: Are they truly barnacles?. Acta Zool. 1992, 73: 323-326.View ArticleGoogle Scholar
- Walker G: Introduction to the Rhizocephala (Crustacea: Cirripedia). Journal of morphology. 2001, 249 (1): 1-8. 10.1002/jmor.1038.View ArticlePubMedGoogle Scholar
- Høeg JT, Glenner H, Shields J: Cirripedia, Thoracica and Rhizocephala (barnacles). Marine Parasites. Edited by: Rohde K. 2005, Wallingford, U. K. & Collingwood, Victoria, Australia: CABI Publishing & CSIRO Publishing, 154-165.Google Scholar
- Glenner H: Cypris metamorphosis, injection and earliest internal development of the Rhizocephalan Loxothylacus panopaei (Gissler). Crustacea: Cirripedia: Rhizocephala: Sacculinidae. Journal of morphology. 2001, 249 (1): 43-75. 10.1002/jmor.1040.View ArticlePubMedGoogle Scholar
- Glenner H, Høeg JT, O'Brien JJ, Sherman TD: The invasive vermigon stage in the parasitic barnacles Loxothylacus texanus and L. panopaei (Sacculinidae): Closing of the rhizocephalan life cycle. Mar Biol. 2000, 136: 249-257. 10.1007/s002270050683.View ArticleGoogle Scholar
- Grygier MJ: Ascothoracida. Crustacés: Géneralités (suite) et systématique (1re partie). Edited by: Forest J. 1996, Paris: Masson, 7: 433-452.Google Scholar
- Grygier MJ, Hoeg JT: Ascothoracida (Ascothoracids). Marine Parasites. Edited by: Rohde K. 2005, Collingwood, Victoria, Australia: CABI Publishing, Wallingford U.K. & CSIRO Publishing, 149-154.Google Scholar
- Hansen HJ: Die cladoceren und cirripedien der plankton expedition. Ergebn Plankton Exped Humboldt-Stift. 1899, 2(G, d): 1-58.Google Scholar
- Grygier MJ: Classe des Thécostracés (Thecostraca Gruvel, 1905). Sous Classe des Facetotecta (Facetotecta Grygier, 1985). Crustacés: Géneralités (suite) et systématique (1re partie). Edited by: Forest J. 1996, Paris: Masson, 7: 425-432.Google Scholar
- Glenner H, Hoeg JT, Grygier MJ, Fujita Y: Induced metamorphosis in crustacean y-larvae: towards a solution to a 100-year-old riddle. BMC biology. 2008, 6: 21-10.1186/1741-7007-6-21.PubMed CentralView ArticlePubMedGoogle Scholar
- Grygier MJ: Facetotecta ('Y larvae'): One day's catch in Okinawa, Japan (Crustacea:Maxillopoda). Mem Queensl Mus. 1991, 31: 335-Google Scholar
- Martin JW, Davis GE: An updated classification of the Recent Crustacea. Nat Hist Mus Los Angeles Sci Ser. 2001, 39: 1-124.Google Scholar
- Glenner H, Hebsgaard MB: Phylogeny and evolution of life history strategies of the parasitic barnacles (Crustacea, Cirripedia, Rhizocephala). Mol Phylogenet Evol. 2006, 41 (3): 528-538. 10.1016/j.ympev.2006.06.004.View ArticlePubMedGoogle Scholar
- Pérez-Losada M, Harp M, Hoeg JT, Achituv Y, Jones D, Watanabe H, Crandall KA: The tempo and mode of barnacle evolution. Mol Phylogenet Evol. 2008, 46 (1): 328-346. 10.1016/j.ympev.2007.10.004.View ArticlePubMedGoogle Scholar
- Pérez-Losada M, Høeg JT, Crandall KA: Unraveling the evolutionary radiation of the Thoracican barnacles using molecular and morphological evidence: A comparison of several divergence time estimation approaches. Syst Biol. 2004, 53 (2): 244-264. 10.1080/10635150490423458.View ArticlePubMedGoogle Scholar
- Pérez-Losada M, Høeg JT, Kolbasov GA, Crandall KA: Reanalysis of the relationships among the Cirripedia and the Ascothoracida and the phylogenetic position of the Facetotecta (Maxillopoda: Thecostraca) using 18S rDNA sequences. J Crust Biol. 2002, 22 (3): 661-669. 10.1651/0278-0372(2002)022[0661:ROTRAT]2.0.CO;2.View ArticleGoogle Scholar
- Glenner H, Grygier MJ, Høeg JT, Jensen PG, Schram FR: Cladistic analysis of the Cirripedia Thoracica (Crustacea: Thecostraca). Zool J Linn Soc. 1995, 114: 365-404. 10.1111/j.1096-3642.1995.tb00121.x.View ArticleGoogle Scholar
- Høeg J: Cypris settlement, kentrogon formation and host invasion in the parasitic barnacle Lernaeodiscus porcellanae (Müller) (Crustacea: Cirripedia: Rhizocephala). Acta Zool. 1985, 66: 1-45.View ArticleGoogle Scholar
- Høeg J, Hosfeld B, Jensen P: TEM studies of lattice organs of cirripede cypris larvae (Crustacea, Thecostraca, Cirripedia). Zoomorphology. 1998, 118: 195-205. 10.1007/s004350050069.View ArticleGoogle Scholar
- Lagersson N, Høeg J: Settlement behavior and antennulary biomechanics in cypris larvae of Balanus amphitrite (Crustacea: Thecostraca: Cirripedia). Mar Biol. 2002, 141: 513-526. 10.1007/s00227-002-0854-1.View ArticleGoogle Scholar
- Spears T, Abele LG, Applegate MA: Phylogenetic study of cirripedes and selected relatives (Thecostraca) based on 18S rDNA sequence analysis. J Crust Biol. 1994, 14 (4): 641-656. 10.2307/1548858.View ArticleGoogle Scholar
- Mizrahi I, Achituv Y, Katcoff DJ, Perl Treves R: Phylogenetic position of Ibla (Cirripedia: Thoracica) based on 18S rDNA sequence analysis. J Crustacean Biol. 1998, 18: 363-368. 10.2307/1549330.View ArticleGoogle Scholar
- Perl-Treves R, Mizrahi L, Katcoff DJ, Achituv Y: Elucidation of the phylogenetic relationships of three thecostracans, Verruca, Paralepas, and Dendrogaster based on 18S rDNA sequences. J Crust Biol. 2000, 20: 385-392. 10.1651/0278-0372(2000)020[0385:EOTPRO]2.0.CO;2.View ArticleGoogle Scholar
- Harris DJ, Maxson L, Braithwaite LF, Crandall KA: Phylogeny of the thoracican barnacles based on 18S rDNA sequences. J Crust Biol. 2000, 20 (2): 393-398. 10.1651/0278-0372(2000)020[0393:POTTBB]2.0.CO;2.View ArticleGoogle Scholar
- Kolbasov GA, Grygier MJ, Høeg JT, Klepal W: External morphology of the two cypridiform ascothoracid-larva instars of Dendrogaster: The evolutionary significance of the two-step metamorphosis and comparison of lattice organs between larvae and adult males (Crustacea, Thecostraca, Ascothoracida). Zool Anz. 2008, 247: 159-183. 10.1016/j.jcz.2007.07.007.View ArticleGoogle Scholar
- Grygier MJ: Classification of the Ascothoracida (Crustacea). Proc Biol Soc Wash. 1987, 100: 452-458.Google Scholar
- Jensen PG, Høeg JT, Bower S, Rybakov AV: Scanning electron microscopy of lattice organs in cyprids of the Rhizocephala Akentrogonida (Crustacea Cirripedia). Can J Zool. 1994, 72: 1018-1026. 10.1139/z94-138.View ArticleGoogle Scholar
- Høeg JT, Kolbasov GA: Lattice organs in y cyprids of the Facetotecta and their significance in the phylogeny of the Crustacea Thecostraca. Acta Zool. 2002, 83: 67-79. 10.1046/j.0001-7272.2001.00100.x.View ArticleGoogle Scholar
- Rybakov AV, Høeg JT, Jensen PG, Kolbasov GA: The chemoreceptive lattice organs in cypris larvae develop from naupliar setae (Thecostraca: Cirripedia, Ascothoracida And Facetotecta. Zool Anz. 2003, 242: 1-20. 10.1078/0044-5231-00084.View ArticleGoogle Scholar
- Bielecki J, Chan BKK, Hoeg JT, Sari A: Antennular sensory organs in cyprids of balanomorphan cirripedes: Standardizing terminology using Megabalanus rosa. Biofouling. 2009, 25 (3): 203-214. 10.1080/08927010802688087.View ArticlePubMedGoogle Scholar
- Lützen J: Amphipoda (amphipods). Marine Parasites. Edited by: Rohde K. 2005, Wallingford U.K. & Collingwood, Victoria, Australia: CABI Publishing & CSIRO Publishing, 165-169.Google Scholar
- Richter S, Scholtz G: Phylogenetic analysis of the Malacostraca (Crustacea). J Zool Syst Evol Research. 2001, 39: 113-136. 10.1046/j.1439-0469.2001.00164.x.View ArticleGoogle Scholar
- Poore G: Peracarida: monophyly, relationships and evolutionary success. Nauplius. 2005, 13 (1): 1-27.Google Scholar
- Lester RJG: Isopoda (isopods). Marine Parasites. Edited by: Rohde K. 2005, Wallingford U.K. & Collingwood, Victoria, Australia: CABI Publishing & CSIRO Publishing, 138-144.Google Scholar
- Huys R, Boxshall GA: Copepod Evolution. 1991, London: The Ray SocietyGoogle Scholar
- Glenner H, Høeg JT: A new motile, multicellular stage involved in host invasion of parasitic barnacles (Rhizocephala). Nature. 1995, 377: 147-150. 10.1038/377147a0.View ArticleGoogle Scholar
- Huys R, Boxshall GA, Lincoln RJ: The tantulocaridan life cycle: The circle closed?. J Crustacean Biol. 1993, 13: 432-442. 10.2307/1548786.View ArticleGoogle Scholar
- Boxshall GA: Tantulocarida (tantulocarids). Marine Parasites. Edited by: Rohde K. 2005, Wallingford, U. K & Victoria, Australia: CABI Publishing & CSIRO Publishing & Collingwood, 147-149.Google Scholar
- Regier JC, Shultz JW, Ganley AR, Hussey A, Shi D, Ball B, Zwick A, Stajich JE, Cummings MP, Martin JW, Cunningham CW: Resolving arthropod phylogeny: exploring phylogenetic signal within 41 kb of protein-coding nuclear gene sequence. Systematic biology. 2008, 57 (6): 920-938. 10.1080/10635150802570791.View ArticlePubMedGoogle Scholar
- Regier JC, Shultz JW, Kambic RE: Pancrustacean phylogeny: hexapods are terrestrial crustaceans and maxillopods are not monophyletic. Proceedings. 2005, 272 (1561): 395-401.Google Scholar
- Mallatt J, Giribet G: Further use of nearly complete 28S and 18S rRNA genes to classify Ecdysozoa: 37 more arthropods and a kinorhynch. Mol Phylogenet Evol. 2006, 40 (3): 772-794. 10.1016/j.ympev.2006.04.021.View ArticlePubMedGoogle Scholar
- Høeg JT, Lützen J: Comparative morphology and phylogeny of the family Thompsoniidae (Cirripedia, Rhizocephala, Akentrogonida), with descriptions of three new genera and seven new species. Zool Scr. 1993, 22: 363-386. 10.1111/j.1463-6409.1993.tb00365.x.View ArticleGoogle Scholar
- Newman WA: Evolution of cirripedes and their major groups. Barnacle biology. Edited by: Southward AJ. 1987, Rotterdam, the Netherlands: A. A. Balkema, 5: 3-42.Google Scholar
- Grygier MJ: Towards a diagnosis of the Facetotecta (Crustacea: Maxillopoda:Thecostraca). Zool Sci. 1991, 8: 1196-Google Scholar
- Moyse J, Jensen PG, Høeg JT, Al Yahya HA: Attachment organs in cypris larvae: using scanning electron microscopy. New frontiers in barnacle evolution. Edited by: Schram FR, Høeg JT. 1995, Rotterdam, the Netherlands: A. A. Balkema, 10: 153-178.Google Scholar
- Kolbasov GA, Høeg JT: Cypris larvae of acrothoracican barnacles (Thecostraca: Cirripedia: Acrothoracica). Zool Anz. 2007, 246: 127-151. 10.1016/j.jcz.2007.03.001.View ArticleGoogle Scholar
- Celis A, Alvarez F, Newman WA, Sumida PYG: Description and phylogenetic significance of the fronto-lateral gland pores and dorsal lattice organs of cyprid larvae of seven species of barnacles. J Crust Biol. 2008, 28: 203-215. 10.1651/0278-0372(2008)028[0203:DAPSOT]2.0.CO;2.View ArticleGoogle Scholar
- Høeg JT, Achituv Y, Chan B, Chan KI, Pérez-Losada M, Gram-Jensen PG: Cypris morphology in the barnacles Ibla and Paralepas (Cirripedia: Thoracica) – Implications for understanding cirripede evolution. J Morphol. 2009, 270: 241-255. 10.1002/jmor.10684.View ArticlePubMedGoogle Scholar
- Katoh K, Kuma K, Toh H, Miyata T: MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 2005, 33 (2): 511-518. 10.1093/nar/gki198.PubMed CentralView ArticlePubMedGoogle Scholar
- Castresana J: Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000, 17 (4): 540-552.View ArticlePubMedGoogle Scholar
- Stamatakis A: RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics (Oxford, England). 2006, 22 (21): 2688-2690. 10.1093/bioinformatics/btl446.View ArticleGoogle Scholar
- Wiens J: Combining data sets with different phylogenetic histories. Syst Biol. 1998, 47: 568-581. 10.1080/106351598260581.View ArticlePubMedGoogle Scholar
- Felsenstein J: Evolutionary trees from DNA sequences: A maximum likelihood approach. J Mol Evol. 1981, 17: 368-376. 10.1007/BF01734359.View ArticlePubMedGoogle Scholar
- Swofford DL: PAUP*: Phylogenetic Analysis Using Parsimony (*and other methods). 2002, Sunderland, MA: Sinauer, 4.0 beta 10Google Scholar
- Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics (Oxford, England). 2003, 19: 1572-1574. 10.1093/bioinformatics/btg180.View ArticleGoogle Scholar
- Posada D, Buckley TR: Model selection and model averaging in phylogenetics: Advantages of Akaike Information Criterion and Bayesian approaches over Likelihood Ratio Tests. Syst Biol. 2004, 53: 793-808. 10.1080/10635150490522304.View ArticlePubMedGoogle Scholar
- Posada D, Crandall KA: Modeltest: testing the model of DNA substitution. Bioinformatics (Oxford, England). 1998, 14 (9): 817-818. 10.1093/bioinformatics/14.9.817.View ArticleGoogle Scholar
- Tavaré S: Some probabilistic and statistical problems in the analysis of DNA sequences. 1986, Providence, RI: Amer. Math. SocGoogle Scholar
- Lewis PO: A likelihood approach to estimating phylogeny from discrete morphological character data. Systematic biology. 2001, 50 (6): 913-925. 10.1080/106351501753462876.View ArticlePubMedGoogle Scholar
- Jukes TH, Cantor CR: Evolution of protein molecules. Mammalian Protein Metabolism. Edited by: Munro HM. 1969, New York, NY: Academic Press, 21-132.View ArticleGoogle Scholar
- Rambaut A, Drummond AJ: Tracer: MCMC trace analysis tool. 2003, Oxford: University of Oxford, [http://evolve.zoo.ox.ac.uk]1.2Google Scholar
- Huelsenbeck JP, Imennov NS: Geographic origin of human mitochondrial DNA: accommodating phylogenetic uncertainty and model comparison. Syst Biol. 2002, 51 (1): 155-165. 10.1080/106351502753475934.View ArticlePubMedGoogle Scholar
- Huelsenbeck JP, Larget B, Miller RE, Ronquist F: Potential applications and pitfalls of Bayesian inference of phylogeny. Syst Biol. 2002, 51 (5): 673-688. 10.1080/10635150290102366.View ArticlePubMedGoogle Scholar
- Felsenstein J: Confidence limits on phylogenies: an approach using the bootstrap. Evolution. 1985, 39: 783-791. 10.2307/2408678.View ArticleGoogle Scholar
- Maddison DR, Maddison WP: MacClade 4: Analysis of Phylogeny and Character Evolution. 2000, Sunderland, MA: Sinauer Associates, 4Google Scholar
- Shimodaira H, Hasegawa M: Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol. 1999, 16 (8): 1114-1116.View ArticleGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.