Poetsworm

Home page of James Skelton

Embedded Metacommunities; a multi scale, multi-species framework for symbiosis ecology

Primary collaborators: Bryan Brown from Virginai Tech (www.faculty.biol.vt.edu/brown/)  and Robert Creed from Appalachian State (http://biology.appstate.edu/faculty-staff/90)

Objectives

  • 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.

metacom

The symbiont infracommunity: Crayfish simultaneously host hundreds of worms from multiple species that compete for resources [8] 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 [12] (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.

Figure 2 - Symbiont niche partitioning. Four functional groups identified by hierarchical clustering from > 3,000 observations of preferred attachment sites for 8 species of worms. Null model permutations of extensive survey data indicate that species within functional groups co-occur far less than expected by chance, suggesting that niche overlap determines symbiont co-occurrence
Figure 2 – Symbiont niche partitioning. Four functional groups identified by hierarchical clustering from > 3,000 observations of preferred attachment sites for 8 species of worms. Null model permutations of extensive survey data indicate that species within functional groups co-occur far less than expected by chance, suggesting that niche overlap determines symbiont co-occurrence

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 [3]. 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 [13]. Although they are not strictly species-specific [14], crayfish worms often prefer particular host species [15], or host sizes [8], 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.

Figure 3 (A) Undergrad researchers use “Ultimate Sampler2000”, a custom built quantitative crayfish sampler, to explore host density and symbiont dynamics in a southern Appalachian stream. (B) Worms are transmitted while hosts fight for shelter in experimental artificial stream channels. (Bottom) Different multi-scale patterns of symbiont diversity under high (black) and low (grey) host density in replicated artificial streams. High host density facilitates species-specific host selection, reducing average symbiont diversity on each host (alpha), and increasing variation in symbiont composition among hosts (beta).
Figure 3 (A) Undergrad researchers use “Ultimate Sampler2000”, a custom built quantitative crayfish sampler, to explore host density and symbiont dynamics in a southern Appalachian stream. (B) Worms are transmitted while hosts fight for shelter in experimental artificial stream channels. (Bottom) Different multi-scale patterns of symbiont diversity under high (black) and low (grey) host density in replicated artificial streams. High host density facilitates species-specific host selection, reducing average symbiont diversity on each host (alpha), and increasing variation in symbiont composition among hosts (beta).

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.

Figure 4 (A) Ordination showing strong correspondence between symbiont infracommunity composition and local host community composition throughout southwest VA. Circles represent site scores for symbiont communities. Colors represent 3 watersheds surveyed. Circle size represents stream size. Large and small text show host and symbiont species scores, respectively. (B) Four years of quantitative survey showed strong seasonal cycles in worm abundance in two streams (red and blue). Line thickness corresponds to crayfish size. (C) Reduced symbiont abundance and diversity where non-native Orconectes crayfish have invaded. Data are from native host species.
Figure 4 (A) Ordination showing strong correspondence between symbiont infracommunity composition and local host community composition throughout southwest VA. Circles represent site scores for symbiont communities. Colors represent 3 watersheds surveyed. Circle size represents stream size. Large and small text show host and symbiont species scores, respectively. (B) Four years of quantitative survey showed strong seasonal cycles in worm abundance in two streams (red and blue). Line thickness corresponds to crayfish size. (C) Reduced symbiont abundance and diversity where non-native Orconectes crayfish have invaded. Data are from native host species.

Literature Cited

  1. Hutchinson G.E. 1959 Homage to Santa Rosalia or why are there so many kinds of animals? American naturalist, 145-159.
  2. Dobson A., Lafferty K.D., Kuris A.M., Hechinger R.F., Jetz W. 2008 Homage to Linnaeus: How many parasites? How many hosts? Proceedings of the National Academy of Sciences 105(Supplement 1), 11482-11489.
  3. Mihaljevic J.R. 2012 Linking metacommunity theory and symbiont evolutionary ecology. Trends in Ecology & Evolution 27(6), 323-329.
  4. Pedersen A.B., Fenton A. 2007 Emphasizing the ecology in parasite community ecology. Trends in ecology & evolution 22(3), 133-139.
  5. Poulin R. 2007 Are there general laws in parasite ecology? Parasitology 134(06), 763-776.
  6. Graham A.L. 2008 Ecological rules governing helminth–microparasite coinfection. Proceedings of the National Academy of Sciences 105(2), 566-570.
  7. Skelton J., Doak S., Leonard M., Creed R.P., Brown B.L. 2016 The rules for symbiont community assembly change along a mutualism‐parasitism continuum. Journal of Animal Ecology 85, 843-853.
  8. Skelton J., Creed R.P., Brown B.L. 2015 A symbiont’s dispersal strategy: Condition-dependent dispersal underlies predictable variation in direct transmission among hosts. Proceedings of the Royal Society B: Biological Sciences 282(1819). (doi:DOI: 10.1098/rspb.2015.2081).
  9. Leibold M.A., Holyoak M., Mouquet N., Amarasekare P., Chase J., Hoopes M., Holt R., Shurin J., Law R., Tilman D. 2004 The metacommunity concept: a framework for multi‐scale community ecology. Ecology Letters 7(7), 601-613.
  10. Thomas M.J., Creed R.P., Skelton J., Brown B.L. 2016 Ontogenetic shifts in a freshwater cleaning symbiosis: consequences for hosts and their symbionts. Ecology 97(6), 1507-1517.
  11. Skelton J., Geyer K.M., Lennon J.T., Creed R.P., Brown B.L. 2016 Multi-scale ecological filters shape the crayfish microbiome. (PeerJ Preprints.
  12. Grinnell J. 1917 The niche-relationships of the California Thrasher. The Auk 34(4), 427-433.
  13. Koepp S.J. 1975 Effects of host ecdysis on population structure of the epizootic branchiobdellid Cambarincola vitrea. Science of Biology Journal 1, 39-42.
  14. Hobbs H.H.J., Holt P.C., Walton M. 1967 The crayfishes and their epizootic ostracod and branchiobdellid associates of the Mountain Lake, Virginia, Region. Proceedings of the United States National Museum 123, 1-84.
  15. Brown B.L., Creed R.P. 2004 Host preference by an aquatic ectosymbiotic annelid on 2 sympatric species of host crayfishes. Journal of the North American Benthological Society 23(1), 90-100. (doi:10.1899/0887-3593(2004)023<0090:hpbaae>2.0.co;2).
  16. Skelton J., Creed R.P., Brown B.L. 2014 Ontogenetic shift in host tolerance controls initiation of a cleaning symbiosis. Oikos 123(6), 677-686.
  17. Farrell K.J., Creed R.P., Brown B.L. 2014 Reduced Densities of Ectosymbiotic Worms (Annelida: Branchiobdellida) on Reproducing Female Crayfish. Southeastern Naturalist 13(3), 523-529. (doi:10.1656/058.013.0312).
  18. Farrell K.J., Creed R.P., Brown B.L. 2014 Preventing overexploitation in a mutualism: partner regulation in the crayfish–branchiobdellid symbiosis. Oecologia 174(2), 501-510.
  19. Skelton J., Farrell K.J., Creed R.P., Williams B.W., Ames C., Helms B.S., Stoekel J., Brown B.L. 2013 Servants, scoundrels, and hitchhikers: current understanding of the complex interactions between crayfish and their ectosymbiotic worms (Branchiobdellida). Freshwater Science 32(4), 1345-1357.
  20. Black T.R., Herleth-King S.S., Mattingly H.T. 2010 Efficacy of Internal PIT Tagging of Small-Bodied Crayfish for Ecological Study. Southeastern Naturalist 9(sp3), 257-266. (doi:10.1656/058.009.s314).
  21. Westhoff J.T., Sievert N.A. 2013 Mortality and Growth of Crayfish Internally Tagged with PIT Tags. North American Journal of Fisheries Management 33(5), 878-881. (doi:10.1080/02755947.2013.815669).