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Trematodes with a Reproductive Division of Labour: Heterophyids Also

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Trematodes with a Reproductive Division of Labour: Heterophyids Also PARA 3913 No. of Pages 10, Model 5G 1 December 2016 International Journal for Parasitology xxx (2016) xxx–xxx 1 Contents lists available at ScienceDirect International Journal for Parasitology journal homepage: www.elsevier.com/locate/ijpara 6 7 3 Trematodes with a reproductive division of labour: heterophyids also 4 have a soldier caste and early infections reveal how colonies become 5 structured a,⇑ b,c b,d a,e 8 Ana E. Garcia-Vedrenne , Anastasia C.E. Quintana , Andrea M. DeRogatis , Christina M. Dover , a a,b a,f 9 Maribel Lopez , Armand M. Kuris , Ryan F. Hechinger 10 a Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, CA 93106, USA 11 b College of Creative Studies, University of California, Santa Barbara, CA 93106, USA 12 c Department of Marine Science and Conservation, Nicholas School of the Environment, Duke University, Durham, NC 27708, USA 13 d Department of Animal Science, University of California, Davis, CA 95616, USA 14 e Virginia-Maryland College of Veterinary Medicine, Blacksburg, VA 24061, USA 15 f Scripps Institution of Oceanography, Marine Biology Research Division, University of California, San Diego, La Jolla, CA 92093, USA 1617 18 article info abstract 3520 21 Article history: Recent findings have extended the documentation of complex sociality to the Platyhelminthes, describing 36 22 Received 17 August 2016 the existence of a reproductive division of labour involving a soldier caste among the parthenitae of 37 23 Received in revised form 7 October 2016 trematode parasites. However, all species examined to date occupy high positions in trematode inter- 38 24 Accepted 7 October 2016 specific dominance hierarchies and belong to two closely related families, the Echinostomatidae and 39 25 Available online xxxx the Philophthalmidae (Superfamily Echinostomatoidea). Further, the two species documented as lacking 40 soldiers also belong to the Echinostomatidae. Here, we examine four species of intermediate dominance, 41 26 Keywords: all belonging to the family Heterophyidae (Superfamily Opisthorchioidea): Euhaplorchis californiensis, 42 27 Sociality Phocitremoides ovale, Pygidiopsoides spindalis and Stictodora hancocki, all of which infect the California 43 28 Colony 29 Soldier caste horn snail, Cerithideopsis californica (=Cerithidea californica). We quantify morphology, distribution and 44 30 Defence behaviour of rediae from fully developed colonies. We also provide information on colony structure for 45 31 Rediae three developing heterophyid colonies to better understand colony development. We discuss the impli- 46 32 Digenea cations of our findings, particularly with respect to how they suggest alternatives to the conclusions of 47 33 Trematoda other researchers concerning the nature of trematode sociality. Our analyses of morphological, distribu- 48 34 tional and behavioural patterns of developed colonies indicate that these heterophyid trematodes have a 49 non-reproductive caste whose function is defence of the colony from invading trematodes. Hence, a sol- 50 dier caste occurs for species lower in dominance hierarchies than previously known, and is present in at 51 least two superfamilies of digenean trematodes, suggesting that selection for a soldier caste may be much 52 more common among the Trematoda than previously recognised. 53 Ó 2016 Published by Elsevier Ltd on behalf of Australian Society for Parasitology. 54 55 56 57 58 1. Introduction morphologically and behaviourally distinct reproductive and 67 non-reproductive castes (Hechinger et al., 2011; Leung and 68 59 A complex social system has recently been documented in dige- Poulin, 2011; Miura, 2012; Nielsen et al., 2014; Garcia-Vedrenne 69 60 nean trematodes (Hechinger et al., 2011; Leung and Poulin, 2011; et al., 2016). Although the non-reproducing caste might have some 70 61 Miura, 2012; Nielsen et al., 2014; Garcia-Vedrenne et al., 2016). other roles (e.g., Lloyd and Poulin, 2012; Galaktionov et al., 2015), 71 62 As in the most complex animal societies (e.g., several types of it is clear that a major role is defence of colonies (Hechinger et al., 72 63 insects (e.g., Wilson, 1971; Aoki, 1977; Crespi, 1992; Kent and 2011; Miura, 2012; Mouritsen and Halvorsen, 2015; Garcia- 73 64 Simpson, 1992; reviewed in Myles, 1999), snapping shrimp Vedrenne et al., 2016). 74 65 (Duffy, 1996), and naked mole-rats, (Jarvis et al., 1981)), the Digenean trematode colonies are formed in the first intermedi- 75 66 parthenita stages of some trematode species live in colonies with ate host, usually a mollusk. The colony is initiated by a single foun- 76 der larva (miracidium) that infects the host, metamorphoses and 77 clonally produces large numbers of daughter parthenitae. Some 78 ⇑ Corresponding author. trematode species have rediae: parthenitae that possess a muscu- 79 E-mail address: [email protected] (A.E. Garcia-Vedrenne). http://dx.doi.org/10.1016/j.ijpara.2016.10.003 0020-7519/Ó 2016 Published by Elsevier Ltd on behalf of Australian Society for Parasitology. Please cite this article in press as: Garcia-Vedrenne, A.E., et al. Trematodes with a reproductive division of labour: heterophyids also have a soldier caste and early infections reveal how colonies become structured. Int. J. Parasitol. (2016), http://dx.doi.org/10.1016/j.ijpara.2016.10.003 PARA 3913 No. of Pages 10, Model 5G 1 December 2016 2 A.E. Garcia-Vedrenne et al. / International Journal for Parasitology xxx (2016) xxx–xxx 80 lar pharynx and a gut. Other species have sporocysts, which lack a Here, we examine four trematode species that belong to the 146 81 pharynx and gut. Both kinds of parthenitae produce more parthen- Family Heterophyidae of the Superfamily Opisthorchioidea (Euhap- 147 82 itae and then dispersive offspring (cercariae), which leave the col- lorchis californiensis, Phocitremoides ovale, Pygidiopsoides spindalis 148 83 ony to infect the next host in the life cycle. Once established, the and Stictodora hancocki).These species form colonies in the Califor- 149 84 colony blocks host reproduction and takes control of the host’s nia horn snail, Cerithideopsis californica (=Cerithidea californica). The 150 85 energy allocation to serve the needs of the colony, primarily divert- California horn snail is host for a diverse trematode guild that is 151 86 ing energy to parasite reproduction (Rothchild and Clay, 1952; characterised by a fairly well-resolved interspecific dominance 152 87 Kuris, 1974; Baudoin, 1975; Hechinger et al., 2009; Lafferty and hierarchy (Kuris, 1990; Sousa, 1993; Hechinger, 2010). Five of the 153 88 Kuris, 2009). The colony commonly occupies the gonad and/or most dominant species in this hierarchy (all in the Superfamily 154 89 digestive gland of the host, taking up a large portion of the host’s Echinostomatoidea) have been documented to have soldiers. The 155 90 soft tissue (10–50%) (e.g., Hurst, 1927; Bernot and Lamberti, heterophyids studied herein have an intermediate position in the 156 91 2008; Hechinger et al., 2009). Given their extensive use and dominance hierarchy (they are subordinate to the echinostomatids 157 92 control of host resources, such conditions would lead to intense and philophthalmids, but can eliminate or prevent infections of 158 93 competition should another trematode invade the same molluscan other, more subordinate, species in the guild (Kuris, 1990)). We 159 94 host. also compare colony structure of a few recent, developing hetero- 160 95 Typically, when two trematode species infect the same host, phyid colonies to fully developed colonies to shed light on the nat- 161 96 one kills the other. These antagonistic interactions are hierarchical. ure of colony development. We discuss the implications of our 162 97 Dominant species fend off invasions or displace established colo- results, including alternative interpretations concerning the nature 163 98 nies of subordinate species. This displacement may be via chemical of trematode sociality. Our analysis of morphology, distribution, 164 99 mechanisms (known for some species with sporocysts (Basch et al., behaviour and colony development of these four heterophyid spe- 165 100 1969; Walker, 1979)), but it most commonly occurs via predation cies indicates that they also have a soldier caste, and that trema- 166 101 by rediae (Lim and Heyneman, 1972; Lie, 1973; Combes, 1982; tode caste structure takes time to develop, becoming more 167 102 Kuris, 1990; Sousa, 1993). Until recently, this antagonism had been pronounced with colony age. 168 103 considered to occur via the actions of ‘‘totipotent” rediae, those 104 that both reproduce and defend the colony (Lim and Heyneman, 2. Materials and methods 169 105 1972; Lie, 1973; Kuris, 1990; Sousa, 1993; but see Lie, 1969). 106 However, recent studies have shown that several trematode 2.1. Study system and sample collection 170 107 species have a division of labour involving a caste of non- 108 reproducing soldiers that are specialised for defence (Hechinger California horn snails, Cerithideopsis californica (=Cerithidea cali- 171 109 et al., 2011; Leung and Poulin, 2011; Miura, 2012; Nielsen et al., fornica), (Potamididae) were collected from Carpinteria Salt Marsh, 172 110 2014; Garcia-Vedrenne et al., 2016). Despite being smaller than Santa Barbara County, California, USA between July 2013 and May 173 111 reproductives, soldiers have relatively large pharynxes to attack 2016. Snails were maintained in the laboratory for up to 7 weeks in 174 112 and kill invaders. Only soldiers readily attack heterospecific
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