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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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