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Social Organization and Caste Formation in Three Additional Parasitic Flatworm Species

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Social Organization and Caste Formation in Three Additional Parasitic Flatworm Species Vol. 465: 119–127, 2012 MARINE ECOLOGY PROGRESS SERIES Published September 28 doi: 10.3354/meps09886 Mar Ecol Prog Ser Social organization and caste formation in three additional parasitic flatworm species Osamu Miura* Oceanography Section, Science Research Center, Kochi University, 200 Monobe, Nankoku, Kochi, 783-8502 Japan ABSTRACT: There are many examples of reproductive division of labor in terrestrial animal societies, but only a few have been reported in aquatic systems. A recent study discovered social organization of a trematode parasite in a marine system which included reproductive and soldier castes. Here I expand that work, reporting on caste formation in 3 species of trematodes infecting the Asian mud snail Batillaria attramentaria, to demonstrate the generality of this phenomenon. I found that the trematodes Philophthalmid sp. I, Philophthalmid sp. II and Acanthoparyphium sp. I have 2 types of morphologically and functionally distinct larval trematode morphs in their colonies. Large morphs were reproductive and filled with embryos, while small morphs had no embryos. Small soldier morphs were disproportionately common in regions within the host where new infections occur, and had relatively large mouthparts. Finally, only small soldier morphs attacked heterospecifics. Division of labor in trematodes is geographically widespread and has now been documented in North America, East Asia and Oceania; this may provide a useful model for comparing ecology and evolution of social organization in animal societies. KEY WORDS: Trematode · Sociality · Caste · Batillaria attramentaria · Philophthalmidae · Acanthoparyphium Resale or republication not permitted without written consent of the publisher INTRODUCTION Grosberg 1996, Ayre & Grosberg 2005) have been reported to exhibit a reproductive division of labor. Societies with castes are common in terrestrial sys- Hechinger et al. (2011) demonstrated that a para- tems, particularly among insects. Hymenopteran in- sitic flatworm, Himasthla sp. B, exhibits social orga - sects such as ants (Wilson 1971), wasps (Matthews nization involving a reproductive caste and a non- 1968, Klahn & Gamboa 1983) and bees (Batra 1964, reproductive soldier caste. Himasthla sp. B is a Michener 1969) show substantial division of labor. tre ma tode that forms colonies in the California horn Termites (Myles 1999), aphids (Aoki 1977, Rhoden & snail Cerithideopsis californica (Hechinger et al. Foster 2002) and thrips (Crespi 1992) have also de - 2011). Trematodes infect snails as their first inter- veloped unique social systems with caste formation. mediate host and asexually produce clone mates Social insects are widely distributed and abundant in (rediae or sporocysts) (Galaktionov & Dobrovolskij terrestrial systems (e.g. May 1989). Social organiza- 2003). Hundreds of redia clone mates can comprise tion is a very successful lifestyle in terrestrial systems a colony in a snail. Rediae produce cercaria larvae (Wilson & Kinne 1990, Chapman & Bourke 2001). In that leave the colony and disperse to continue the contrast, sociality involving separate castes of mobile life cycle. Typically, all generations are diploid, and organisms seems to be rare in aquatic systems. Only those resulting from infection with one miracidia Caribbean snapping shrimps (Duffy 1996) and a larva are genetically identical (Cable 1971). Hech - North American sea anemone (Ayre 1982, Ayre & inger et al. (2011) showed that about half of the *Email: [email protected] © Inter-Research 2012 · www.int-res.com 120 Mar Ecol Prog Ser 465: 119–127, 2012 rediae in Himasthla sp. B colonies do not produce Acan tho paryphium sp. I) possess soldier and repro- cercariae and are specialized for attacking and ductive castes. These species were used for subse- killing conspecific or heterospecific competitors. quent morphological and behavioral examination. Thus, for the first time, they documented a repro- The larval stages of these parasites are de scribed ductive di vision of labor in a parasitic flatworm (Hechinger 2007), but do not have species binomials involving a non-reproductive soldier caste. Repro- associated as the adult worms in the final host have ductive rediae produce numerous offspring, and are not been described. Although Philophthalmid sp. II large and inactive. Soldier rediae do not produce are known to have 3 genetically distinct cryptic spe- offspring, are small but have relatively large mouth- cies (Miura et al. 2005), they were not distinguished parts, are more active, are aggressive towards non- in the present study. colony conspecifics and heterospecifics, and are disproportionally common at sites within the host where new infections occur. Morphological analyses Trematodes are common in freshwater and marine ecosystems. Diverse guilds of trematodes infect a Under a stereomicroscope, larval trematodes (re- variety of marine and freshwater snails (Yamaguti diae) were separated from the dissected host. I used 1975). Although individual trematodes are small, random grid numbers to collect 50 to 100 individuals their colonies can comprise >40% the weight of an (ind.) from each colony. I fixed the rediae with 10% infected snail (Hechinger et al. 2009) and their total hot formalin. Digital pictures of each morph were biomass within an ecosystem can exceed that of top taken using a compound microscope with an Olym- predators in some estuaries (Kuris et al. 2008). Con- pus DP 70 camera system at 20 to 40× magnification sidering the high diversity and biomass of these for body total length and maximum width and 100× para sites, it is possible that social organization is for pharynx length and width. For the 3 trematode also a pervasive and successful lifestyle in aquatic species, I measured the body and pharynx size of 46 systems. Further, as with social insects, trematodes to 118 ind. for several colonies: 9 colonies for may provide a rich system to test hypotheses about Philophthalimid sp. I, 8 for Philophthalmid sp. II and the ecology and evolution of sociality. Hechinger et 6 for Acantho paryphium sp. I, for a total of 1677 al. (2011) predicted the widespread occurrence of rediae. All measurements were obtained using tre ma tode castes, and I demonstrate this in 3 more image analysis software WinRoof Ver. 5.02 (Mitani species. In the present study, I investigate morpho- Corporation). I calculated body and pharynx vol- logical and behavioral features of 3 trematodes umes of redia using the approximation of a cylinder. infecting an Asian mud snail to evaluate the exis- I recognized 2 redia morphs with clear morphologi- tence of caste formation. I focus on quantifying cal disparity (Figs. 1 & 2). I postulated that these are basic morphological differences (body and mouth- the soldier and reproductive morphs shown in part size), attack rates toward heterospecifics and Hechinger et al. (2011). I used general linear mixed conspecifics, caste numbers in colonies, and morph models to compare redia body sizes in different distribution in snails. castes. Colonies were treated as a random effect. I have deposited the voucher specimens at the Tohoku University Museum (TUMC Nos. 111184 to MATERIALS AND METHODS 111198). Sample collection Attack rates The mud snail Batillaria attramentaria was collec- ted at Mangoku Bay in Miyagi prefecture Japan To evaluate aggression of each redia morph (38° 25’ 59.5”N, 141°24’ 46.2”E) between August against its self, conspecific and heterospecific colo - 2011 to April 2012. Adult snails (~3 cm shell length) nies, I performed 4 treatments for each colony; 30 ind. were dissected under a stereomicroscope. The tre - of the soldier morph and 20 ind. of the reproductive ma tode colonies were sampled in blind fashion from morph were collected from a colony, and 10 ind. of the snails. Trematode species were identified using the reproductive morph were collected from different morphological characters following Hechinger (2007). colonies (as conspecific enemies). I also collected Observations suggested that 3 species of trematodes 20 ind. of rediae (reproductive morph) from a differ- (Philophthalmid sp. I, Philophthalmid sp. II and ent trematode species, Cercaria batillariae (as hetero - Miura: Social organization in three Asian trematodes 121 Fig. 1. Reproductive and soldier rediae of (a,d) Philophthalmid sp. I (PHI1), (b,e) Philophthalmid sp. II (PHI2) and (c,f) Acantho - paryphium sp. I (ACAN). Soldier rediae (a,b,c) in insets of (d,e,f) at the same scale as reproductive rediae PHI1 PHI2 ACAN a 500 1000 400 400 800 300 300 600 200 200 400 Body width (µm) 100 100 200 0 0 0 1000 2000 3000 1000 2000 3000 4000 5000 500 1000 1500 2000 Body length (µm) b 100 80 80 70 70 80 60 60 60 50 50 40 40 40 30 30 Frequency 20 20 20 10 10 0 0 0 6.0 6.5 7.0 7.5 8.0 8.5 6.0 6.5 7.0 7.5 8.0 8.5 9.0 6.5 7.0 7.5 8.0 Soldier Reproductive Soldier Reproductive Soldier Reproductive 3 Log10 volume (µm ) Fig. 2. (a) Body length and width of the rediae and (b) distribution of redia size. Philophthalmid sp. I (PHI1), Philophthalmid sp. II (PHI2) and Acanthoparuphium sp. I (ACAN). Horizontal grey bars indicate the range of the 2 caste groups 122 Mar Ecol Prog Ser 465: 119–127, 2012 specific enemies). Experiments consisted of different RESULTS rediae being placed together in a 0.3 ml plastic well with 0.1 ml of RPMI-1640 medium. There were 4 Morphology treatments: (1) 10 soldiers and 10 reproductives from the same colony, (2) 10 soldiers and 10 C. batillariae Each of the 3 trematode species exhibited 2 distinct heterospecifics, (3) 10 soldiers and 10 reproductives redia morphs (Fig. 1). Reproductive rediae were al - from different colonies and (4) 10 reproductives and ways filled with several early to late-stage embryos, 10 C. batillariae hetero specifics. The experiments while none of the 150 soldier rediae (50 ind. for each were conducted during daytime at room temperature species) that I inspected under high magnification (20 to 25°C).
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