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Divergent Evolutionary Pathways and Host Shifts Among the Commensal Pontoniine Shrimps: a Preliminary Analysis Based on Selected Indo-Pacific Species

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Divergent Evolutionary Pathways and Host Shifts Among the Commensal Pontoniine Shrimps: a Preliminary Analysis Based on Selected Indo-Pacific Species Org Divers Evol (2015) 15:369–377 DOI 10.1007/s13127-014-0198-y ORIGINAL ARTICLE Divergent evolutionary pathways and host shifts among the commensal pontoniine shrimps: a preliminary analysis based on selected Indo-Pacific species Qi Kou & Xin-Zheng Li & Tin-Yam Chan & Ka Hou Chu Received: 17 July 2014 /Accepted: 15 December 2014 /Published online: 30 December 2014 # Gesellschaft für Biologische Systematik 2014 Abstract As the most species-rich subfamily of Caridea, commensal pontoniine shrimps with similar hosts or niches Pontoniinae Kingsley, 1878 is well-known for its great diver- are identified, with a host-shifting hypothesis proposed for sity in morphology, lifestyle and habitat. However, the phy- cavity-inhabiting pontoniines based on molecular data in con- logeny of Pontoniinae has been poorly studied since it was junction with morphological and ecological evidence. erected, and there are many taxonomic and evolutionary con- troversies remained unresolved. Among these controversies, Keywords Palaemonidae . Pontoniinae . Phylogeny . the relationship between the commensal pontoniine shrimps Evolution . Commensalism . Host shift and their hosts is the issue of most concern. Herein, a total of 26 Indo-Pacific pontoniine species from 23 genera, including both free-living and commensal taxa associated with different marine organisms from five phyla, are selected to preliminar- ily explore the differentiation process accompanied with the reciprocal natural selections between them and their hosts. Introduction Based on the molecular phylogenetic analyses, two major clades, representing the ‘primitive groups’ and ‘derived The family Palaemonidae Rafinesque, 1815, which currently groups’, and several subgroups related to the hosts are well comprises more than 980 species, is the most species-rich recovered, which are also supported in morphology. family in Caridea (De Grave and Fransen 2011). Additionally, several possible evolutionary pathways of those Palaemonidae consists of two subfamilies, Palaemoninae Rafinesque, 1815 and Pontoniinae Kingsley, 1878. Electronic supplementary material The online version of this article Compared with the Palaemoninae, which is widespread in (doi:10.1007/s13127-014-0198-y) contains supplementary material, marine, brackish and freshwater in the tropical and temperate which is available to authorized users. : regions (Ashelby et al. 2012), the Pontoniinae is mostly re- Q. Kou X.<Z. Li (*) stricted to tropical and subtropical marine habitats but with Institute of Oceanology, Chinese Academy of Sciences, 7 Nanhai much more species. To date, the Pontoniinae includes over Road, Qingdao 266071, China e-mail: [email protected] 110 genera and 600+ species, distributed from intertidal zone to deep sea, and the exact diversity is supposed to be far more Q. Kou e-mail: [email protected] than this (Li et al. 2007). Apart from a limited number of free- living species, pontoniine shirmps are generally associated T.<Y. C han with various marine organisms (Li 1993). Their hosts contain Institute of Marine Biology and Center of Excellence for the Oceans, sponges, cnidarians, echinoderms, molluscs, polychaetes, as- National Taiwan Ocean University, 2 Pei-Ning Road, Keelung 202, Taiwan cidians and even other crustaceans and are sometimes highly e-mail: [email protected] specific (Bruce 1994; Hayashi and Ohtomi 2001; Bruce and Okuno 2006; Komai et al. 2010). Presumably, such a variety K. H. Chu of commensal lifestyles and habitats in Pontoniinae contrib- Simon F.S. Li Marine Science Laboratory, School of Life Sciences, The Chinese University of Hong Kong, Shatin, N. T., Hong Kong utes to the enormous morphological diversity nowadays (Li e-mail: [email protected] and Liu 1997; Kou et al. 2013a). 370 Q. Kou et al. On account of the extremely high diversity, the classifica- morphological evidence to support the conclusion. Finally, we tion of the subfamily Pontoniinae based solely on morpholog- will try to preliminarily elucidate the diversification of the ical characters is inevitably subjective and probably inaccu- studied pontoniine taxa, which is often accompanied with host rate. Consequently, additional host and habitat data are used to shifts, by integrated morphological, ecological and the current assist in delineating the growing pontoniine taxa. However, molecular data, and provide new insights to the classification for a number of the commensal pontoniine shrimps sharing of this controversial subfamily. similar niches, their morphology appears evidently different, and they are speculated to arise from divergent evolutionary pathways (Li and Liu 1997; Marin and Chan 2006). Besides, Materials and methods many homoplastic and specialized morphological characters of the commensal pontoniine shrimps also perplex the taxon- Sample collection omists, making the traditional taxonomic studies a tough work. A total of 26 Indo-Pacific species from 23 genera of the As a resultful and hopeful approach to resolving the knotty Pontoniinae, plus one out-group species Macrobrachium problems of systematics, however, the molecular nipponense (De Haan, 1849 [in De Haan, 1833–1850]) from phylogenetics on the pontoniines has been limited within the Palaemoninae were included in this study. The ingroup only a small number of taxa included. Mitsuhashi et al. taxa included both free-living and those species which are (2007) examined the systematic status of the two species- commensally associated with different marine organisms, poor palaemonoidean families Gnathophyllidae Dana, 1852 aiming to achieve a comprehensive coverage on the different and Hymenoceridae Ortmann, 1890 with eight pontoniine lifestyles and habitats of the pontoniine shrimps. All speci- genera, indicating an affinity between these two families and mens were identified by the second or third authors, who are Pontoniinae. Fransen and Reijnen (2012) reevaluated the sys- the experts on caridean taxonomy. Then, the specimens were tematic position of two bivalve-associated pontoniine genera preserved in absolute alcohol prior to DNA extraction. The Lacertopontonia Marin, 2011 and Chernocaris Johnson, 1967 details of all the specimens are listed in Table 1. based on morphological and molecular data, suggesting that both genera should be considered as synonyms of the genera DNA extraction, PCR amplification and sequencing Conchodytes Peters, 1852. Kou et al. (2013a) investigated the phylogeny of the Periclimenes complex, focusing on eluci- Total genomic DNA was extracted from abdomen muscle or dating the polyphyletic status of the genus Periclimenes and pleopod (5–20 mg) using a QIAamp DNA Mini Kit (Qiagen). the phylogenetic relationships among Periclimenes and 15 The DNA was eluted in 100 μl of sterile distilled H2O(RNase related genera. Except for the meager studies mentioned free) and stored at −20 °C. The extracted DNAwas checked by 1– above, the systematics of the Pontoniinae was rarely touched 1.5 % agarose gel electrophoresis and ethidium bromide staining. upon, leaving the subfamily a highly controversial taxon in Although effective, the nuclear protein coding genes were phylogeny and evolution. performed to be a bit too conservative at the generic level, and Kou et al. (2013a) preliminarily deduced the probable sometimes, the phylogenetic analysis could not obtain a differentiation process of the pontoniine shrimps and sug- strongly supported topology at several subbranches in our gested that a comprehensive molecular phylogenetic study previous work (see Kou et al. 2013a). In view of this, nuclear ideally in conjunction with the morphological, lifestyle and genes were not mainly used in the present study. Instead, two habitat characteristics is required to infer the natural phylog- mitochondrial genes (12S and 16S rRNA) and one nuclear eny. Thus, in this study, 26 Indo-Pacific species from 23 gene (histone 3) were utilized to infer the phylogeny. affiliated genera of the Pontoniinae are selected as the subject Partial segments of 12S rRNA (~350 bp), 16S rRNA investigated, including both free-living species and commen- (~480 bp) and histone 3 (~350 bp) genes were amplified by sal species associated with different marine organisms from polymerase chain reaction (PCR). Amplifications were carried five phyla. Firstly, we will explore their phylogeny utilizing out in a reaction mix containing 1–5 μloftemplateDNA,5μlof three loci, viz. the mitochondrial 12S and 16S ribosomal RNA 10×PCR buffer (Mg2+ plus, Takara), 4 μlofdNTP(10mM (rRNA) and the nuclear histone three genes, which are sug- each), 1.5 μl of each primer (10 mM), 1 μl of Taq polymerase −1 gested suitable for the phylogenetic analysis at the generic (5 U ml , Takara) and sterile distilled H2O to a total volume of level of decapod (Toon et al. 2009) and proved to be capable 50 μl. For the 12S rRNA segments, PCR amplifications were of solving a series of evolutionary problems in the carried out using primers 12S–f/r (Mokady et al. 1994), with the Palaemoninae (Ashelby et al. 2012; Kou et al. 2013b). following cycling profile: initial denaturation for 10 min at 94 °C, Secondly, we will attempt to answer the question, ‘Did those followed by 35 to 40 cycles of denaturation at 94 °C for 30 s, commensal pontoniine shrimps sharing similar hosts evolve annealingat48°Cfor40s,extensionat72°Cfor30sandafinal through divergent evolutionary pathways or not?’ and find extension at 72 °C for 10 min. For the amplification of the 16S Divergent evolutionary pathways and host shifts among pontoniids 371 Table
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