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A framework for using phoresy to assess ecological transition into parasitism and mutualism

Abstract

Phoresy is commonly considered to be a commensal interaction, in which one species hitches a ride upon a different species for dispersal among resource patches. Despite being ubiquitous, phoretic interactions are poorly investigated, limiting our current understanding of its ecological and evolutionary consequences. Furthermore, phoresy can be a precursor for different types of symbiotic interactions, including parasitism, yet empirical tests for this long-standing hypothesis are rare. Using burying beetles and their phoretic mites as a model phoresy, I review and synthesise the ecological processes driving the transition of commensalism to parasitism and/or mutualism. I argue that density-dependent effects, resource availability, life history stage, and community context all play significant roles, both during and after the transportation stage. Understanding how these factors drive variation in interaction outcomes in rapidly changing environments presents one of the major challenges in evolutionary ecology. Finally, I highlight some important future directions and research areas that will advance our understanding of the ecology and evolution of phoresy and symbiotic interactions as a whole.

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References

  • Agrawal AA, Ackerly DD, Adler F, Arnold AE, Cáceres C, Doak DF et al (2007) Filling key gaps in population and community ecology. Front Ecol Environ 5:145–152

    Article  Google Scholar 

  • Bartlow AW, Agosta SJ (2021) Phoresy in animals: review and synthesis of a common but understudied mode of dispersal. Biol Rev 96:223–246

    Article  Google Scholar 

  • Bronstein JL (2001) The costs of mutualism. Am Zool 41:825–839

    Google Scholar 

  • Bronstein JL (2015) Mutualism, 1st edn. Oxford University Press, Oxford, UK

    Book  Google Scholar 

  • Brooks DR, McLennan DA (2002) The nature of diversity : an evolutionary voyage of discovery. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Canitz J, Sikes DS, Knee W, Baumann J, Haftaro P, Steinmetz N et al (2022) Cryptic diversity within the Poecilochirus carabi mite species complex phoretic on Nicrophorus burying beetles: Phylogeny, biogeography, and host specificity. Mol Ecol 31:658–674

  • Cotter SC, Topham E, Price AJ, Kilner RM (2010) Fitness costs associated with mounting a social immune response. Ecol Lett 13:1114–1123

    CAS  Article  Google Scholar 

  • Crook M (2014) The dauer hypothesis and the evolution of parasitism: 20 years on and still going strong. Int J Parasitol 44:1–8

    Article  Google Scholar 

  • De Gasperin O, Kilner RM (2015) Friend or foe: inter-specific interactions and conflicts of interest within the family. Ecol Entomol 40:787–795

    Article  Google Scholar 

  • de Gasperin O, Kilner RM (2016) Interspecific interactions and the scope for parent-offspring conflict: high mite density temporarily changes the trade-off between offspring size and number in the burying beetle, Nicrophorus vespilloides. PLoS One 11(3):e0150969

  • Duarte A, Cotter SC, De Gasperin O, Houslay TM, Boncoraglio G, Welch M et al (2017) No evidence of a cleaning mutualism between burying beetles and their phoretic mites. Sci Rep 7:1–12

    Article  Google Scholar 

  • Duarte A, Welch M, Swannack C, Wagner J, Kilner RM (2017b) Strategies for managing rival bacterial communities: Lessons from burying beetles. J Anim Ecol 87:414–427

    Article  Google Scholar 

  • Gupta S, Borges R (2021) Hopping on: Conspecific traveller density within a vehicle regulates parasitic hitchhiking between ephemeral microcosms. J Anim Ecol 90:899–908

    Article  Google Scholar 

  • Gupta S, Kumble A, Dey K, Bessière JM, Borges R (2021) The scent of life: Phoretic nematodes use wasp volatiles and carbon dioxide to choose functional vehicles for dispersal. J Chem Ecol 47:139–152

    CAS  Article  Google Scholar 

  • Herrera P, Schuster L, Wentrup C, König L, Kempinger T, Na H, Schwarz J, Köstlbacher S, Wascher F, Zojer M, Rattei T, Horn M (2020) Molecular causes of an evolutionary shift along the parasitism–mutualism continuum in a bacterial symbiont. Proc Natl Acad Sci USA 117:21658–21666

    CAS  Article  Google Scholar 

  • Holte A, Houck M, Collie N (2001) Potential role of parasitism in the evolution of mutualism in astigmatid mites: Hemisarcoptes cooremani as a model. Exp Appl Acarol 25:97–107

    CAS  Article  Google Scholar 

  • Houck MA, Cohen AC (1995) The potential role of phoresy in the evolution of parasitism: radiolabelling (tritium) evidence from an astigmatid mite. Exp Appl Acarol 1912(19):677–694

    Article  Google Scholar 

  • Houck MA, OConnor BM (1991) Ecological and evolutionary significance of phoresy in the Astigmata. Annu Rev Entomol 36:611–636

    Article  Google Scholar 

  • Kilner RM, Hinde CA (2012) Parental-Offspring Conflict. In: Royle NJ, Smiseth PT, Kölliker M (eds) The Evolution of Parental Care. Oxford University Press, Oxford, UK, pp 119–132

    Google Scholar 

  • Konwerski S, Gutowski JM, Błoszyk J (2020) Patterns of distribution of phoretic deutonymphs of Uropodina on longhorn beetles in Białowieża Primeval Forest, Central Europe. Diversity 12:239

  • Kuczyński L, Radwańska A, Karpicka-Ignatowska K, Laska A, Lewandowski M, Rector BG, Majer A, Raubic J, Skoracka A (2020) A comprehensive and cost-effective approach for investigating passive dispersal in minute invertebrates with case studies of phytophagous eriophyid mites. Exp Appl Acarol 82:17–31

    Article  Google Scholar 

  • Lang JM, Benbow ME (2013) Species interactions and competition. Nat Educ Knowl 4(4):8

    Google Scholar 

  • Luong L, Mathot K (2019) Facultative parasites as evolutionary stepping-stones towards parasitic lifestyles. Biol Lett 15:20190058

  • Mathis KA, Bronstein JL (2020) Our current understanding of commensalism. Annu Rev Ecol Evol Syst 51:167–189

    Article  Google Scholar 

  • Mountcastle AM, Ravi S, Combes SA (2015) Nectar vs. pollen loading affects the tradeoff between flight stability and maneuverability in bumblebees. Proc Natl Acad Sci USA 112:10527–10532

    CAS  Article  Google Scholar 

  • Nehring V, Teubner H, König S (2019) Dose-independent virulence in phoretic mites that parasitize burying beetles. Int J Parasitol 49:759–767

    Article  Google Scholar 

  • Otronen M (1988) The effects of body size on the outcome of fights in burying beetles (Nicrophorus). Ann Zool Fennici 25:191–201

    Google Scholar 

  • Payne JA (1965) A summer carrion study of the baby pig Sus Scrofa Linnaeus. Ecology 46:592–602

    Article  Google Scholar 

  • Perotti M, Braig H (2009) Phoretic mites associated with animal and human decomposition. Exp Appl Acarol 49:85–124

    Article  Google Scholar 

  • Pukowski E (1933) Ökologische untersuchungen an Necrophorus F. Zeitschr Morph Ökol Tiere 27:518–586

    Article  Google Scholar 

  • Queller DC, Strassmann JE (2018) Evolutionary conflict. Annu Rev Ecol Evol Syst 49:73–93

    Article  Google Scholar 

  • Royle NJ, Hopwood PE, Head ML (2014) Burying beetles. Curr Biol 23:R907–R909

    Article  Google Scholar 

  • Schedwill P, Geiler AM, Nehring V (2018) Rapid adaptation in phoretic mite development time. Sci Rep 8:16460

    Article  Google Scholar 

  • Schrader M, Jarrett BJM, Kilner RM (2015) Parental care masks a density-dependent shift from cooperation to competition among burying beetle larvae. Evolution 69:1077–1084

    Article  Google Scholar 

  • Schwarz HH, Koulianos S (1999) When to leave the brood chamber? Routes of dispersal in mites associated with burying beetles. Ecology and Evolution of the Acari. Springer, Netherlands, Dordrecht, pp 323–331

    Chapter  Google Scholar 

  • Schwarz HH, Müller JK (1992) The dispersal behaviour of the phoretic mite Poecilochirus carabi (Mesostigmata, Parasitidae): adaptation to the breeding biology of its carrier Necrophorus vespilloides (Coleoptera, Silphidae). Oecologia 89:487–493

    Article  Google Scholar 

  • Scott MP (1998) The ecology and behavior of burying beetles. Annu Rev Entomol 43:595–618

    CAS  Article  Google Scholar 

  • Scott MP (1994) Competition with flies promotes communal breeding in the burying beetle, Nicrophorus tomentosus. Behav Ecol Sociobiol 34:367–373

  • Sun S-J, Kilner RM (2020) Temperature stress induces mites to help their carrion beetle hosts by eliminating rival blowflies. eLife 9:e55649

    CAS  Article  Google Scholar 

  • Sun S-J, Rubenstein DR, Chen B-F, Chan S-F, Liu J-N, Liu M et al (2014) Climate-mediated cooperation promotes niche expansion in burying beetles. eLife 9:e55649

  • Sun S-J, Horrocks NPC, Kilner RM (2019) Conflict within species determines the value of a mutualism between species. Evol Lett 3:185–197

    Article  Google Scholar 

  • Sun S-J, Catherall AM, Pascoal S, Jarrett BJM, Miller SE, Sheehan MJ et al (2020) Rapid local adaptation linked with phenotypic plasticity. Evol Lett 4:345–359

    Article  Google Scholar 

  • Sun S-J, Kilner RM (2019) Cryptic host specialisation within Poecilochirus carabi mites explains population differences in the extent of co-adaptation with their burying beetle Nicrophorus vespilloides hosts. bioRxiv https://doi.org/10.1101/641936

  • White PS, Morran L, de Roode J (2017) Phoresy. Curr Biol 27:R578–R580

    CAS  Article  Google Scholar 

  • Wilson DS (1983) The effect of population structure on the evolution of mutualism: a field test involving burying beetles and their phoretic mites. Am Nat 121:851–870

    Article  Google Scholar 

  • Wilson DS, Knollenberg WG (1987) Adaptive indirect effects: the fitness of burying beetles with and without their phoretic mites. Evol Ecol 1:139–159

    Article  Google Scholar 

Download references

Acknowledgements

I would like to thank Ming-Yang Chang for comments that improved the manuscript, the Kilner Group at the University of Cambridge, and the Cambridge Commonwealth, European and International Trust for supporting the PhD fellowship with Taiwan Cambridge Scholarship.

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Correspondence to Syuan-Jyun Sun.

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Sun, SJ. A framework for using phoresy to assess ecological transition into parasitism and mutualism. Symbiosis 86, 133–138 (2022). https://doi.org/10.1007/s13199-022-00830-7

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  • DOI: https://doi.org/10.1007/s13199-022-00830-7

Keywords

  • Interspecific interactions
  • Burying beetles
  • Phoretic mites
  • Mutualism
  • Parasitism