Crayfish throughout North America, Europe and Asia are hosts to small leech-like annelids called crayfish worms (Annelida: Branchiobdellida; Figure 1). Hundreds of worms belonging to several genera and multiple species often vie for space and resources on a single host. The worms’ entire lives are spent attached to crayfish, from egg to adult, and transmission occurs almost exclusively via direct host to host contact. Thus each crayfish body represents an island colonized by diverse and interactive assemblage of symbiotic worms. Recent work has shown that this system is extremely amenable to observational and experimental studies because the organisms are common, widespread, these ecto-symbionts can be observed and quantified non-destructively, and crayfish and their worms are easily maintained in the laboratory (Skelton_etal_2013). By applying elements of general ecological theory and rigorous experimentation, studies of crayfish and branchiobdellidans are providing a new understanding of 1) how interactions between hosts and their symbionts change with context, 2) how hosts manage their symbionts throughout their lives, 3) how host resistance mediates interactions among symbiont species, and 4) how competition among symbionts drives transmission among potential hosts.
Context is (almost) everything: Textbook treatments of symbiosis present a steadfast typology based on the outcomes of an interaction for both parties. For instance, if the interaction benefits only one party and harms the other, the symbiosis is a “parasitism”. If it benefits both, it is a “mutualism”. This typology of symbiosis is popular because it is tractable, but it is problematic. The outcomes of symbioses are rarely fixed, and more often depend upon the ever-changing context of interactions. Thus an understanding of how symbiosis influences an organism’s ecology and evolution requires a flexible symbiosis continuum framework that accounts for changing outcomes under varying contexts. Crayfish worms can benefit their host by cleaning harmful scum composed of bacteria, algae, fungi etc., from the host’s body, which in turn increases the hosts growth rates and survival. However, crayfish worms may also incur costs by feeding on host tissues (Brown_etal_2012). Factors that tip the balance between costs and benefits determine the immediate outcomes of the symbiosis between crayfish and their worms. Field experiments using multiple crayfish and worm species demonstrated that the effects of crayfish worms on their hosts change with the number of worms living on a host; from positive effects at low to intermediate numbers to negative effects at higher numbers (Brown_etal_2012; Figure 2). As worm numbers increased, increasing damages to host tissues outweighed the benefits of cleaning. Thus the interaction appears mutualistic or parasitic, depending on the abundance of symbionts on a given host. But symbiont abundance is only one element of the context surrounding hosts and their symbionts.
Ontogeny adds complexity: Changes to an organism’s biology during aging and development, or ontogeny, adds another dimension to the context of symbiotic interactions. An interaction may be beneficial at one life stage and detrimental at another. Experimental examination of the effects of two species of crayfish worms on their hosts at multiple life stages showed that juvenile crayfish received no benefit from hosting worms, whereas both species of crayfish worms enhanced the growth rates of adult crayfish (Thomas et al 2016). This result is probably explained by changes in the molting rate during host development. Young crayfish molt frequently, whereas older crayfish rarely molt. Thus, young crayfish receive no benefit of cleaning because molting complete relieves them of harmful scum, whereas older crayfish benefit from their cleaning symbionts. The symbiosis only becomes mutualistic when molting frequency slows during adulthood, and accumulating scum becomes problematic.
Control mechanisms and the maintenance of mutualism: Mutualisms are everywhere and affect nearly every organism on Earth, yet the evolution of mutualisms and their persistence through evolutionary time may seem paradoxical. Natural selection should favor individuals that cheat their partners to gain increased benefits at the expense of their partners. Adaptive responses that limit cheating and over-exploitation and/or favor beneficial interactions offer a resolution to the apparent paradox. The crayfish worm symbiosis changes from not beneficial to beneficial during host development (Thomas et al. 2016), suggesting that crayfish could maximize the life-long net outcome of symbiosis by controlling when they contract symbiotic worms. Crayfish use specific grooming behaviors to control the initiation of their partnership with crayfish worms. Young crayfish used the small claws of their anterior walking legs to methodically pluck worms from their bodies, and often ingested them SEE MOVIE HERE. However, at a specific body size (a proxy for crayfish age), this behavioral response disappears (Skelton_etal_2016; Skelton_etal_2014). Moreover, worm behavior changes in response to changing host responses. Worms on young crayfish remain tucked away from prying claws, whereas worms on older crayfish move into more conspicuous locations (Skelton_etal_2014). This work is the first experimental demonstration that partner control mechanisms may be adjusted during development to maximize the life-long benefit of symbiotic partnerships, providing a new understanding of how mutually beneficial symbioses can remain ecologically and evolutionarily stable.
A symbiont’s dispersal stragy: While it is clear that crayfish can exert controls over their symbionts, what strategies might a symbiont use to maximize its own fitness? From a symbiont’s perspective, a host population or community is analogous to a patchy and heterogeneous landscape, like an island archipelago. Hosts vary in the quantity and quality of resources they offer to symbionts, and symbionts that share a host must compete for limited resources. Studies of free-living organisms have demonstrated that selectively choosing when to disperse based on the quality of a given habitat, or the degree of competition in that habitat, can maximize the fitness of the individual. Put simply, it is good to be choosy about where one lives. In contrast, most studies of symbionts focus only on the opportunities a symbiont has to disperse, and assume that all symbionts will disperse according to a fixed probability. Simply, symbionts are seen as not being choosy about their hosts and are thought to move from host to host indiscriminately. By imagining a choosy symbiont that switches hosts discriminately based on host quality and competition with other symbionts, we produced a model that can accurately predict transmission frequency and magnitude during experimental encounters between infected and non-infected crayfish (Skelton etal 2015). The model accounted for factors identified by my field study to affect symbiont reproductive success (i.e. host size, and competition for microhabitat), and made predictions based on the assumption that symbionts would only disperse when the probability of reproductive success on their current host was below a minimum threshold value. Permutation-based null models demonstrated that predictions based on condition-dependent dispersal were much better than those based on the commonly held assumption of a fixed transmission rate. Thus, this work clearly shows us that future attempts to understand or predict transmission dynamics in natural populations should consider the context of transmission opportunities, as well as their frequency (Skelton etal 2015).
Linking changing outcomes with symbiont community assembly: The study of symbioses has historically been focused on pairwise interaction between species. While pairwise frameworks are tractable, they are often insufficient for symbioses of realistic complexity, which often involve simultaneous interactions among many species. Based on principals from “community ecology”, my colleagues and I are developing a conceptual framework for predicting how the importance of interactions among symbionts changes with the effects of symbionts on their hosts. Classical community ecology predicts that low colonization rates lead to communities of low diversity and consequently weak interactions among species. In contrast, high colonization rates should lead to diverse communities that are characterized by strong species interactions such as competition. Thus interactions among symbionts are expected to become increasingly important during crayfish development, as crayfish no longer resist symbiont colonization and subsequently colonization rates increase. Support for this hypothesis came from a combined field and experimental laboratory study (Skelton_etal_2016; Figure 3). Only a few specialized worm species could colonize and persist on young and highly resistant crayfish. These worms were small and capable of evading crayfish grooming efforts by tucking away into inaccessible crevices. These diminutive worms typical of young crayfish had no detectable influence on one another; i.e. there were no interactions among symbionts of young crayfish. However, when host resistance was relaxed as crayfish grew older and benefited from their association with worms, additional symbiont species were able to colonize and interactions between symbionts became important. On older crayfish larger worm species could colonize and prey upon smaller species, and more species competed for space. Thus exploration of the crayfish cleaning system provides a demonstration that the changing outcomes of symbiosis can have direct and indirect effects on the assembly of symbiont communities and future work must account for changing outcomes in symbiotic interactions during symbiont community assembly.