Social organization in a flatworm: trematode parasites form soldier and reproductive castes

Abstract

In some of the most complex animal societies, individuals exhibit a cooperative division of labour to form castes. The most pronounced types of caste formation involve reproductive and non-reproductive forms that are morphologically distinct. In colonies comprising separate or mobile individuals, this type of caste formation has been recognized only among the arthropods, sea anemones and mole-rats. Here, we document physical and behavioural caste formation in a flatworm. Trematode flatworm parasites undergo repeated clonal reproduction of 'parthenitae' within their molluscan hosts forming colonies. We present experimental and observational data demonstrating specialization among trematode parthenitae to form distinct soldier and reproductive castes. Soldiers do not reproduce, have relatively large mouthparts, and are much smaller and thinner than reproductives. Soldiers are also more active, and are disproportionally common in areas of the host where invasions occur. Further, only soldiers readily and consistently attack heterospecifics and conspecifics from other colonies. The division of labour described here for trematodes is strongly analogous to that characterizing other social systems with a soldier caste. The parallel caste formation in these systems, despite varying reproductive mode and taxonomic affiliation, indicates the general importance of ecological factors in influencing the evolution of social behaviour. Further, the 'recognition of self ' and the defence of the infected host body from invading parasites are comparable to aspects of immune defence. A division of labour is probably widespread among trematodes and trematode species encompass considerable taxonomic, life history and environmental diversity. Trematodes should therefore provide new, fruitful systems to investigate the ecology and evolution of sociality.

Parasite diversity and coinfection determine pathogen infection success and host fitness

“…Whereas such reductions may have only weak effects on individual host fitness, likely because parasite-mediated damage occurs during the initial infection stage (40), competitive effects among parasites could nonetheless cause population-level reductions in pathogen transmission. In this system, for instance, a decrease in parasite persistence in intermediate amphibian hosts will likely reduce transmission to vertebrate definitive hosts (often birds or mammals), ultimately lowering parasite abundance-a pattern that will be further enhanced if parasites also behave antagonistically within other hosts in the life cycle (50).…”

Interference competition in entomopathogenic nematodes: male Steinernema kill members of their own and other species

“…There is evidence of physical displacement in helminths, especially bulky cestodes inhabiting vertebrate guts (Haukisalmi and Henttonen, 1993;Behnke et al, 2001). Best documented are the interspecific interactions, including predation, between larval trematodes in snails (Lie et al, 1968;Lim and Heyneman, 1972;Hechinger et al, 2011). Homosexual rape has been documented in acanthocephalans, where cementing of the male victim's genital region effectively removed it from the reproductive population (Abele and Gilchrist, 1977;Hassanine and Al-Jahdali, 2008).…”

“…There is some evidence for the involvement of chemicals -a so-called ''crowding factor'' in intraspecific interactions amongst cestodes (Roberts, 2000). Chemical interactions are ubiquitous in microparasites -for example, bacteriocins are produced by bacteria to kill closely related species (Riley and Wertz, 2002;Mideo, 2009 in the snail intermediate host: the rediae of many echinostome species attack and consume rediae and sporocysts of other trematode species, thereby eliminating subordinate species from the snail (Lie et al, 1968;Lim and Heyneman, 1972;Hechinger et al, 2011). In solitary species of parasitoid insects a host can support only one individual.…”

Two ‘new’ renicolid trematodes (Trematoda: Digenea: Renicolidae) from the California horn snail, Cerithidea californica (Haldeman, 1840) (Gastropoda: Potamididae)

“…Such attention is warranted because, as noted in the introduction, the mass of parthenitae in their first intermediate host is comprised of individuals that cooperatively live together to reproduce and operate the castrated host phenotype. Hence, they can be understood as comprising a colony or society (Hechinger et al 2011b). The degree of sociality can be developed so far as to involve a reproductive division of labor among parthenitae including the formation of a non-reproducing soldier caste (Hechinger et al 2011b;Leung & Poulin 2011;Miura 2012).…”

“…Further, we include more information than is typical concerning the entire group of sporocysts that comprise an infection. This is particularly warranted given the recent recognition that parthenitae in first intermediate hosts can be understood as comprising a colony or society-given that they represent groups of individuals that cooperatively live together to reproduce and operate the castrated host phenotype (see Hechinger et al 2011b). …”