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.

Figure 1.

Secondary morph and primary morph redia dimorphism of the trematode, Himasthla sp. B (HIMB). Secondary morphs are putative soldiers and primary morphs are putative reproductives. (a) A secondary morph next to a primary morph that contains five developed dispersive offspring (cercariae). (b) Close-up of a secondary morph indicating the large pharynx (ph), collar (co) and posterior appendages (ap). (c) Body width versus length for 173 secondary morphs (red circles) and 143 primary morphs (blue diamonds) from seven colonies. Secondary morphs and primary morphs have very different width to length relationships (general linear model using log₁₀-transformed variables: full model R² = 0.97, p < 0.0001; interaction p < 0.0001, F_1,17 = 118; 95% CI for exponents: secondary morphs, −0.21, −0.031; primary morphs, 0.48, 0.65). (d) Secondary morphs overlap with primary morphs in absolute pharynx size, and the 68% average size decrease is not significant (Poisson regression: p = 0.22, χ² = 1.5, d.f. = 1, n = 316). (e) Secondary morph pharynx size relative to body size is 22 times larger than for primary morphs (PReg on × 10⁴ data: p = 0.011, χ² = 6.4, d.f. = 1). These data represent morphs from all colonies, but analyses controlled for any effects of individual colony. Electronic supplementary material, figures S2 and S3 present individual data for each colony. Scale bars (a,b) 0.2 mm.

Figure 2.

Himasthla sp. B (HIMB) secondary morph and primary morph redia in vitro activity rates. (a) Mean absolute body movement rates, and (b) mean proportional body movement for secondary morphs and primary morphs from 11 different trials, each with individuals from a different colony. Each datum represents mean individual movement of up to 20 randomly selected individuals of each caste from each colony observed at three times. Statistics are from paired t-tests using trials as replicates. Dotted lines connect data from same trial (colony). (a) t₁₀ = 3.1, p = 0.011. (b) t₁₀ = 4.3, p = 0.016.

Figure 3.

Himasthla sp. B (HIMB) secondary morph rediae readily attack heterospecifics and non-kin conspecifics whereas primary morphs do not. (a) The mean number of attacks by each secondary morph observed 2 h after placing 15 or 20 secondary morphs from each of 11 colonies with the same amount of (i) secondary morph rediae from the same colony, (ii) heterospecific (E. californiensis-EUHA) rediae (t₁₀ = 5.7, p = 0.0002), or (iii) conspecific secondary morphs from two other colonies (t₁₀ = 3.9, p = 0.003; t₁₀ = 4.8, p = 0.0008). Statistics reflect paired t-tests comparing attack rates to those on ‘self’. The two trials where secondary morphs did not attack both conspecifics were also trials with the lowest attack rates in the heterospecific treatment. Electronic supplementary material, figure S4 presents the actual number of attacks, additional detail, and the results for the additional heterospecific treatments. (b) The mean number of attacks by each morph observed 2 h after placing secondary morphsand primary morphs with 60 heterospecific (EUHA) rediae. The left pair pits an approximately equivalent biomass of primary morphs or secondary morphs against the heterospecifics (t₁₀ = 9.7, p = 0.0001), while the right pair pits an equivalent number (t₁₀ = 9.5, p = 0.0001). In (a) and (b), paired t-tests used trials as replicates, and dotted lines connect data from same trial (colony).

Figure 4.

Himasthla sp. B (HIMB) secondary morph rediae attacking heterospecifics and conspecific secondary morphs from other colonies. (a) A secondary morph swallowing a heterospecific (E. californiensis-EUHA), the posterior end of which is visible in the secondary morph's pharynx cavity (unlabelled black arrow). (b) A secondary morph has lacerated the side of a heterospecific (EUHA), and is ingesting the heterospecific's offspring (the black eyes of which are visible in the secondary morph's intestine). (c) A HIMB secondary morph attacking a heterospecific (Parorchis acanthus, PARO) secondary morph. (d) A secondary morph attacking a primary morph of the heterospecific, PARO. (e) A HIMB secondary morph ingesting a HIMB secondary morph from a different colony. The posterior end of the attacked secondary morph (unlabelled black arrow) fills the anterior 40% of the attacker's intestine. All photos taken through a normal bright field compound microscope, sometimes using phase rings for contrast. scale bars, 0.2 mm.

Figure 5.

Himasthla sp. B (HIMB) secondary morph and primary morph redia caste numbers given colony size, and distribution throughout infected snail bodies. (a) The number of primary morphs weakly increased with infected host body size (Poisson regression (PReg): R²_L = 0.064, p = 0.059, χ² = 3.6, d.f. = 1, n = 49). (b) The number of secondary morphs disproportionately increased with the number of primary morphs (PReg: R²_L = 0.54, p < 0.0001, χ² = 57.9, d.f. = 1, n = 51). (c) The distribution of all individuals in the three regions of the host for 51 HIMB colonies (PReg: overall heterogeneity, p < 0.0001, χ² = 662, d.f. = 2). (d) Secondary morphs were more dispersed throughout the host body than were primary morphs and comprised almost all of the individuals furthest from the colony locus in the gonad region (GLM linear contrast p < 0.0001, F_1,90 = 312). In (c,d), boxes indicate 25th and 75th percentiles, whiskers indicate 10th and 90th percentiles, and the horizontal bars indicate medians.