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PeerJ
2016 Jan 01;4:e1786. doi: 10.7717/peerj.1786.
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From commensalism to parasitism in Carapidae (Ophidiiformes): heterochronic modes of development?
Parmentier E
,
Lanterbecq D
,
Eeckhaut I
.
Abstract
Phenotypic variations allow a lineage to move into new regions of the adaptive landscape. The purpose of this study is to analyse the life history of the pearlfishes (Carapinae) in a phylogenetic framework and particularly to highlight the evolution of parasite and commensal ways of life. Furthermore, we investigate the skull anatomy of parasites and commensals and discuss the developmental process that would explain the passage from one form to the other. The genus Carapus forms a paraphyletic grouping in contrast to the genus Encheliophis, which forms a monophyletic cluster. The combination of phylogenetic, morphologic and ontogenetic data clearly indicates that parasitic species derive from commensal species and do not constitute an iterative evolution from free-living forms. Although the head morphology of Carapus species differs completely from Encheliophis, C. homei is the sister group of the parasites. Interestingly, morphological characteristics allowing the establishment of the relation between Carapus homei and Encheliophis spp. concern the sound-producing mechanism, which can explain the diversification of the taxon but not the acquisition of the parasite morphotype. Carapus homei already has the sound-producing mechanism typically found in the parasite form but still has a commensal way of life and the corresponding head structure. Moreover, comparisons between the larval and adult Carapini highlight that the adult morphotype "Encheliophis" is obtained by going beyond the adult stage reached by Carapus. The entrance into the new adaptive landscape could have been realised by at least two processes: paedomorphosis and allometric repatterning.
Figure 1. Phylogram of Carapini based on the Bayesian analysis.Phylogram showing the results of a Bayesian analysis on the full data set (six genes + morphological characteristics). The values above and below the branches indicate the posterior probabilities obtained during the Bayesian search (six genes + morphological characteristics; partition active) and ML Metaga search (six genes; unpartitioned data set), respectively. The structures of the skulls of the Carapidae are illustrated on the right. FP, French Polynesia; M, Madagascar, Me, Mediterranean.
Figure 2. Phylogram showing the alternative hypothesis obtained in some analysis.In this phylogram, Carapus mourlani is the sister group of (C. boraborensis (C. acus, C. bermudensis)). The values above the branches indicate the posterior probabilities obtained during ML MetaGA search (six genes; partitioned data set).
Figure 3. Cladorgram illustrating the results obtained during an MP search on the morphological data where a backbone constraint has been imposed on the analysis.The backbone constraint highlighted by bold branches imposes the best result obtained with molecular data (see Fig. 1). The search includes rare species for which no molecular data exist. The hosts are drawn at the bases of the clades. The best ML probabilities concerning the symbiotic status of ancestors of clades are indicated above the branches. Considered symbiotic status were: free living (FL), commensal of bivalves (CB), commensal of holothuroids (CH), commensal of ascidiaceans (CA), opportunistic commensal (i.e., more than two classes as hosts; OC), parasite of holothuroids (PH) and opportunistic parasite (i.e., more than two classes as hosts; OP). The best ML probabilities concerning the characteristics of the swim bladder of ancestors of clades are indicated below the branches. Considered characteristics of the swim bladder were: insertion with a long tendon (LT), insertion with a short tendon (ST), presence of the tendon hook system (THS).
Figure 4. Left lateral view of different Carapini skulls.Left lateral views of the skull in different (A) larvae and (B) adult carapid species. 1, Carapus homei; 2, Carapus mourlani; 3, Carapus boraborensis; 4, Encheliophis gracilis. See results section for the numbers.
Capella-Gutiérrez,
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses.
2009, Pubmed
Capella-Gutiérrez,
trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses.
2009,
Pubmed
Colleye,
Interspecific variation of calls in clownfishes: degree of similarity in closely related species.
2011,
Pubmed
Dumont,
Morphological innovation, diversification and invasion of a new adaptive zone.
2012,
Pubmed
Edgar,
MUSCLE: multiple sequence alignment with high accuracy and high throughput.
2004,
Pubmed
Eeckhaut,
Effects of Holothuroid Ichtyotoxic Saponins on the Gills of Free-Living Fishes and Symbiotic Pearlfishes.
2015,
Pubmed
,
Echinobase
Elliott,
Molecular phylogenetic evidence for the evolution of specialization in anemonefishes.
1999,
Pubmed
Felsenstein,
CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP.
1985,
Pubmed
Grant,
CULTURAL INHERITANCE OF SONG AND ITS ROLE IN THE EVOLUTION OF DARWIN'S FINCHES.
1996,
Pubmed
Helaers,
MetaPIGA v2.0: maximum likelihood large phylogeny estimation using the metapopulation genetic algorithm and other stochastic heuristics.
2010,
Pubmed
Huelsenbeck,
Potential applications and pitfalls of Bayesian inference of phylogeny.
2002,
Pubmed
Kishino,
Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea.
1989,
Pubmed
Lagardère,
Aspects of sound communication in the pearlfish Carapus boraborensis and Carapus homei (Carapidae).
2005,
Pubmed
,
Echinobase
Lewis,
A likelihood approach to estimating phylogeny from discrete morphological character data.
2001,
Pubmed
Li,
RNF213, a new nuclear marker for acanthomorph phylogeny.
2009,
Pubmed
Miya,
Major patterns of higher teleostean phylogenies: a new perspective based on 100 complete mitochondrial DNA sequences.
2003,
Pubmed
Parmentier,
Sound production mechanism in carapid fish: first example with a slow sonic muscle.
2006,
Pubmed
Parmentier,
Sound-producing mechanisms and recordings in Carapini species (Teleostei, Pisces).
2003,
Pubmed
,
Echinobase
Posada,
MODELTEST: testing the model of DNA substitution.
1998,
Pubmed
Ronquist,
MrBayes 3: Bayesian phylogenetic inference under mixed models.
2003,
Pubmed
Schluter,
Ecology and the origin of species.
2001,
Pubmed
Schluter,
Evidence for ecological speciation and its alternative.
2009,
Pubmed
Schwarz,
The locomotory system of pearlfish Carapus acus: what morphological features are characteristic for highly flexible fishes?
2012,
Pubmed
Slabbekoorn,
Bird song, ecology and speciation.
2002,
Pubmed
Thompson,
The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.
1997,
Pubmed
Vandewalle,
Distinctive anatomical features of the branchial basket in four carapidae species (ophidiiformi, paracanthopterygii).
1998,
Pubmed