Life-History Differences among Coral Reef Sponges Promote Mutualism or Exploitation of Mutualism by Influencing Partner Fidelity Feedback

Abstract

Mutualism can be favored over exploitation of mutualism when interests of potential heterospecihc partners are aligned so that individual organisms are beneficial to each others' continued growth, survival, and reproduction, that is, when exploitation of a particular partner individual is costly. A coral reef sponge system is particularly amenable to field experiments probing how costs of exploitation can be influenced by life-history characteristics. Pairwise associations among three of the sponge species are mutually beneficial. A fourth species, Desmapsamma anchorata, exploits these mutualisms. Desmapsamma also differs from the other species by growing faster, fragmenting more readily, and suffering higher mortality rates. Evaluating costs and benefits of association in the context of the complex life histories of these asexually fragmenting sponges shows costs of exploitation to be high for the mutualistic species but very low for this essentially weedy species. Although it benefits from association more than the mutualist species, by relying on their superior tensile strength and extensibility to reduce damage by physical disturbance, exploitation is favored because each individual host is of only ephemeral use. These sponges illustrate how life-history differences can influence the duration of association between individuals and, thus, the role of partner fidelity in promoting mutualism.Keywords: sponges, mutualism, partner fidelity, asexual fragmentation, weed strategies, exploitation.Why some species participate in mutualisms while other species exploit mutualisms remains one of the more intriguing questions about interspecific interactions (e.g., (2000) showed that partner interests can align when benefits are symmetrical to the partners, partner species differ in their resource preferences, and successful transmission of a symbiont depends on a long-lived host. Likewise, Yu (2001) stressed the importance of reliable reassembly and the original benefit-donor (or its offspring) receiving the reciprocated benefit. Finally, a model by Foster and Wenseleers (2006) identified high benefit-to-cost ratios for heterospecific interactions, high within-species relatedness, and high between-species fidelity as helping mutualisms withstand the threat of exploitation.In common among many of these mutualism-promoting factors is that they align interests of species by increasing how beneficial an individual (or clone or colony) of one species is to the continued survival, growth, and reproduction of a particular individual of the partner species. If fitness benefits are gained as long as the association is maintained, an exploiter risks damaging itself if it damages its partner, favoring mutualism without need for special sanctions against exploiters (i.e., "passive retaliation" in the sense of Bull and Rice [1991]). This has been referred to as "partner fidelity" by Bull and Rice (1991) and Sachs et al. (2004) and as "community of interest" by Leigh (2001) and has played a prominent role in discussions of

The evolution of mutualism

“…Biologists concerned with how cheating is suppressed have focused largely on symbioses: as we have seen, they have learned how such symbioses are maintained. True, some symbioses, such as those between figs and their pollinating wasps (Herre et al, 2008) or between mutualistic sponges (Wulff, 2008), are parasitized, sometimes heavily, by third parties. How these parasites are limited to tolerable levels is an open question.…”

“…Sponges of the parasite species grow faster and survive better when adhering to a sponge of one of the mutualist species, thanks largely to the mutualists' superior strength. Sponges of the mutualist species, however, grow more slowly and die faster when adhered to by the parasite (Wulff, 2008). Only the parasite's hit-and-run strategy lets it escape the consequences of the harm it inflicts on its partners.…”

“…Mutualisms whose participants share in a common action offering scope for cheating [Mullerian mimicry among butterflies to simplify education of predators, parasitized by palatable Batesian mimics: Fisher, 1930] B. Mutualisms with division of labour 1. Long-term mutualisms (symbioses) a. Mutualisms enforced by transmission of symbionts from a host to its offspring [organelles in eukaryote cells: Eberhard, 1980] b. Mutualisms enforced by partner fidelity [sponges that fuse to pool capacities to resist different hazards for their common good: Wulff, 1997Wulff, , 2008 Howe, 1986] pollinators. The former are more like long-term business contracts; the latter are more like that between mobile buyers and the shopkeepers competing for their custom.…”

There are many ways to be a mutualist: Endophytic fungus reduces plant survival but increases population growth

“…Vertical transmission creates feedbacks by extending species interactions through successive host generations and stabilizes mutualisms by reducing the fitness of partners that fail to cooperate (Ewald 1987, Foster andWenseleers 2006). Some observations support a positive relationship between the rate of vertical transmission and the strength of mutualism across host organisms (Wulff 2008). In addition, experimental tests, while rare, have shown that benefits conferred by symbionts increase when vertical transmission can occur Bull 2005, Stewart et al 2005a).…”

The rules for symbiont community assembly change along a mutualism–parasitism continuum

“…As a consequence of the simultaneous costs and benefits of symbiosis, the net outcome of symbiosis for crayfish is context-dependent as ecological context shifts the balance of the costs and benefits, similar to many other well-studied mutualistic associations (e.g. Thompson & Pellmyr 1992;Johnson, Graham & Smith 1997;Johnstone & Bshary 2002;Wulff 2008;Palmer et al 2010;Yang & Rudolf 2010;Yule, Miller & Rudgers 2013). The net effect of branchiobdellidans on their host changes with the rate of sediment and biofilm accumulation (Lee, Kim & Choe 2009;Thomas, Creed & Brown 2013;Ames, Helms & Stoeckel 2015), symbiont density (Brown et al 2012) and host age (Skelton, Creed & Brown 2014;Thomas 2014).…”