- Unify patch-based ecological theory and symbiosis ecology to clarify terminology and solidify testable hypotheses grounded in established theory
- Identify key ecological processes at multiple scales in symbiotic systems
- Link key processes across scales, from individual symbionts to expansive heterogeneous landscapes
Recent work, primarily in parasitology, has recognized the need for comprehensive approaches that incorporates webs of interactions occurring over multiple temporal and spatial scales to explain patterns of symbiont diversity [3-7]. This realization mirrors the paradigm shift that community ecology experienced with the advent of the “metacommunity” era [3, 9]. In fact, communities of symbionts inhabiting the individual “host islands” that comprise a host community more closely resemble heuristic metacommunity island models than most systems of free-living organisms! But, there are a few twists: 1) unlike inanimate islands or habitat patches, hosts are responsive elements across ecological and evolutionary time scales, and 2) symbiont metacommunities are embedded in the metacommunities of their hosts, adding layers of complexity that require a comprehensive conceptual framework to tame. Inspired by advances in community ecology and experience in several host/symbiont systems, my colleagues and I are developing just such a framework (see Figure 1). Using the crayfish-crayfish worm model system, my work draws from this framework to test salient hypotheses that are grounded in solid ecological theory.
The symbiont infracommunity: Crayfish simultaneously host hundreds of worms from multiple species that compete for resources  and prey on one another [7, 10]. Moreover, recent molecular methods and field experiments revealed dozens of microbial taxa interacting with crayfish worms, creating complex patterns of diversity across spatial scales from tissues to watersheds [11; crayfish microbiome]. The importance of symbiont interactions increases throughout the host’s life, as colonization and reproduction lead to higher symbiont diversity and abundance, and enhance inter- and intra- specific interactions among symbionts [7, 10]. We are discovering that, despite limited host-based resources, as many as 7 worm species can coexist on one crayfish host because the worms spatially partition the host’s body, similar to Grinnel’s original conceptualization of the niche  (Figure 2). Future efforts will relate patterns of functional diversity and phylogenetic diversity across continental spatial scales to test competing hypotheses of character displacement vs. species sorting to explain niche partitioning in a diverse symbiont clade.
The symbiont metacommunity: For obligate symbionts, a host community is a dynamic and heterogeneous archipelago amidst a sea of uninhabitable wastelands. Transmission of symbionts is analogous to dispersal among patches in modern metacommunity frameworks . The opportunities and risks of dispersal are contingent on properties of the host community such as density, diversity, and composition. Crayfish worms are horizontally transmitted among hosts during host-host contact . Although they are not strictly species-specific , crayfish worms often prefer particular host species , or host sizes , and crayfish have variable tolerance to worms across crayfish species and life-stages [7, 16-19]. As a result, crayfish worms exhibit complex dispersal strategies to evade competition and host resistance, and maximize life-time fitness [8, 16]. Current work is combining field surveys with laboratory experiments to test hypotheses derived from metacommunity theory that relate dispersal rate and patch heterogeneity to multi-scale patterns of symbiont diversity (Figure 3). Future efforts will use established mark/recapture methods [20, 21] and newly available micro-PIT tags to observe these dynamics in situ.
Host metacommunities and processes that transcend scales: The most important contribution of the Embedded Metacommunity framework will be to link observations at the scale of individuals – the units of selection and muse of organismal biologists – to processes that operate at broader scales. Understanding how multi-scale processes are linked will help us predict how local communities of hosts and symbionts will be affected by broad-scale disturbances such as habitat destruction, climate change, and species invasions.
Patterns of crayfish worm species composition are surprisingly stable over decadal timescales, despite dramatic intra-annual cycles in total abundance (Figure 4; Skelton et al. in review). Spatial patterns of symbiont diversity are largely explained by differences in host species composition among localities, illustrating the influence of host metacommunity dynamics on local symbiont diversity. Simultaneously, observed symbiont abundance and diversity are lower at sites recently invaded by introduced Orconectes crayfish (Figure 4C). Thus, regional connectivity and human activities may interact to negatively affect local symbiont communities. Future work will use our already established methodologies including artificial stream channels, in situ experiments utilizing flow-through field enclosures and PIT tag mark-recapture efforts, to tease apart interacting effects of host species, host dispersal, and local habitat on local and regional symbiont diversity.
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