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Chapter Seven - Sexually transmitted infections in natural populations: what have we learnt from beetles and beyond?

from Part I - Understanding within-host processes

Published online by Cambridge University Press:  28 October 2019

By
Ben Ashby ,
Jordan E. Jones ,
Robert J. Knell  and
Gregory D.D. Hurst
Edited by
Kenneth Wilson ,
Andy Fenton  and
Dan Tompkins
Kenneth Wilson
Affiliation:
Lancaster University
Andy Fenton
Affiliation:
University of Liverpool
Dan Tompkins
Affiliation:
Predator Free 2050 Ltd
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Summary

Sexually transmitted infections (STIs) can be found in a range of hosts. Their epidemiology is predicted to vary with mean and variance in number of mating partners and, in more refined models, contact and social structure. Weak dependence of mating rate on host density leads to a prediction of density-independent dynamics, including the possibility that sterilising infections could drive their hosts extinct. Infection’s impact on the host is predicted to select for mate choice against infected partners and reduced mating rates. We examine these predictions against STIs in nature, with a particular focus on studies of beetle–ectoparasitic mite interactions. The Adalia bipunctata–Coccipolipus interaction has given rich insights, with ease of scoring infection and mating activity in natural populations enabling detailed documentation of dynamics. Laboratory study has allowed precise estimation of transmission parameters to inform models and focused analysis of behaviour. These studies have confirmed the core impact of mating rate on STI dynamics, but revealed unexpected drivers such as food supply (positively driving mating rate) and sex ratio (enhancing spread and producing male-biased prevalence), alongside constraints on spread from host phenology.

Keywords

ectoparasiteladybirdmating systemphenologyseasonal epidemicssexually transmitted infectionSTI
Type
Chapter
Information
Wildlife Disease Ecology
Linking Theory to Data and Application
 , pp. 187 - 222
Publisher: Cambridge University Press
Print publication year: 2019

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References

Abbot, P. & Dill, L.M. (2001) Sexually transmitted parasites and sexual selection in the milkweed leaf beetle, Labidomera clivicollis. Oikos, 92, 91–100.Google Scholar
Adamo, S.A., Kovalko, I., Easy, R.H. & Stoltz, D. (2014) A viral aphrodisiac in the cricket Gryllus texensis. Journal of Experimental Biology, 217, 1970–1976.Google Scholar
Alexander, H.M. & Maltby, A. (1990) Anther-smut infection of Silene alba caused by Ustilago violacea: factors determining fungal reproduction. Oecologia, 84, 249–253.Google Scholar
Amiri, E., Meixner, M.D. & Kryger, P. (2016) Deformed wing virus can be transmitted during natural mating in honey bees and infect the queens. Scientific Reports, 6, 33065.Google Scholar
Anderson, R.M. & May, R.M. (1991) Infectious Diseases of Humans: Dynamics and Control. Oxford: Oxford University Press.Google Scholar
Apari, P., De Sousa, J.D. & Müller, V. (2014) Why sexually transmitted infections tend to cause infertility: an evolutionary hypothesis. PLoS Pathogens, 10, e1004111.Google Scholar
Ashby, B. & Boots, M. (2015) Coevolution of parasite virulence and host mating strategies. Proceedings of the National Academy of Sciences of the United States of America, 112, 13,290–13,295.Google Scholar
Ashby, B. & Gupta, S. (2013) Sexually transmitted infections in polygamous mating systems. Philosophical Transactions of the Royal Society B, 368, e20120048.Google Scholar
Augustine, D.J. (1998) Modelling Chlamydia–koala interactions: coexistence, population dynamics and conservation implications. Journal of Applied Ecology, 35, 261–272.Google Scholar
Bateman, A.J. (1948) Intra-sexual selection in Drosophila. Heredity, 2, 349–368.Google Scholar
Bauch, C.T. & McElreath, R. (2016) Disease dynamics and costly punishment can foster socially imposed monogamy. Nature Communications, 7, 11219.Google Scholar
Baverud, V., Nystrom, C. & Johansson, K.E. (2006) Isolation and identification of Taylorella asinigenitalis from the genital tract of a stallion, first case of a natural infection. Veterinary Microbiology, 116, 294–300.Google Scholar
Boots, M. & Knell, R.J. (2002) The evolution of risky behaviour in the presence of a sexually transmitted disease. Proceedings of the Royal Society of London B, 269, 585–589.Google Scholar
Brown, A. & Grice, R. (1984) Isolation of Chlamydia psiltaci from koalas (Phascolarctos cinereus). Australian Veterinary Journal, 61, 413–413.Google Scholar
Chahroudi, A., Permar, S. & Pandrea, I. (2014) Chapter 13 – SIV transmission in natural hosts A2 – Ansari, Aftab A. In: Silvestri, G. (ed.), Natural Hosts of SIV. Amsterdam: Elsevier.Google Scholar
Cockram, F. & Jackson, A. (1974) Isolation of a Chlamydia from cases of keratoconjunctivitis in koalas. Australian Veterinary Journal, 50, 82–83.Google Scholar
Cohen, M.S. (1998) Sexually transmitted diseases enhance HIV transmission: no longer a hypothesis. Lancet, 351, 5–7.Google Scholar
Eames, K.T.D. & Keeling, M.J. (2002) Modeling dynamic and network heterogeneities in the spread of sexually transmitted diseases. Proceedings of the National Academy of Sciences of the United States of America, 99, 13,330–13,335.Google Scholar
Escallón, C., Becker, M.H., Walke, J.B., et al. (2017) Testosterone levels are positively correlated with cloacal bacterial diversity and the relative abundance of Chlamydiae in breeding male rufous-collared sparrows. Functional Ecology, 31, 192–203.Google Scholar
Ezenwa, V.O., Etienne, R.S., Luikart, G., Beja-Pereira, A. & Jolles, A.E. (2010) Hidden consequences of living in a wormy world: nematode-induced immune suppression facilitates tuberculosis invasion in African buffalo. American Naturalist, 176, 613–624.Google Scholar
Fauvergue, X. (2013) A review of mate-finding Allee effects in insects: from individual behavior to population management. Entomologia Experimentalis et Applicata, 146, 79–92.Google Scholar
Gascoigne, J., Berec, L., Gregory, S. & Courchamp, F. (2009) Dangerously few liaisons: a review of mate-finding Allee effects. Population Ecology, 51, 355–372.Google Scholar
Getz, W.M. & Pickering, J. (1983) Epidemic models: thresholds and population regulation. American Naturalist, 121, 892–898.Google Scholar
Grassl, J., Peng, Y., Baer-Imhoof, B., et al. (2017) Infections with the sexually transmitted pathogen Nosema apis trigger an immune response in the seminal fluid of honey bees (Apis mellifera). Journal of Proteome Research, 16, 319–334.Google Scholar
Grassly, N.C., Fraser, C. & Garnett, G.P. (2005) Host immunity and synchronized epidemics of syphilis across the United States. Nature, 433, 417–421.Google Scholar
Gupta, S., Anderson, R.M. & May, R.M. (1989) Networks of sexual contacts – implications for the pattern of spread of HIV. AIDS, 3, 807–817.Google Scholar
Haddrill, P.R., Majerus, M.E.N. & Shuker, D.M. (2013) Variation in male and female mating behaviour among different populations of the two-spot ladybird, Adalia bipunctata (Coleoptera: Coccinellidae). European Journal of Entomology, 110, 87–93.Google Scholar
Haddrill, P.R., Shuker, D.M., Amos, W., Majerus, M.E.N. & Mayes, S. (2008) Female multiple mating in wild and laboratory populations of the two-spot ladybird, Adalia bipunctata. Molecular Ecology, 17, 3189–3197.Google Scholar
Hagos, A., Abebe, G., Buscher, P., Goddeeris, B.M. & Claes, F. (2010) Serological and parasitological survey of dourine in the Arsi-Bale highlands of Ethiopia. Tropical Animal Health and Production, 42, 769–776.Google Scholar
Hamilton, W.D. (1990) Mate choice near or far? American Zoologist, 30, 341–352.Google Scholar
Handasyde, K.A. (1986) Factors affecting reproduction in the female koala “Phascolarctos cinereus”. PhD thesis, Monash University.Google Scholar
Handsfield, H.H., Lipman, T.O., Harnisch, J.P., Tronca, E. & Holmes, K.K. (1974) Asymptomatic gonorrhea in men. New England Journal of Medicine, 290, 117–123.Google Scholar
Hart, B.L., Korinek, E. & Brennan, P. (1987) Postcopulatory genital grooming in male-rats – prevention of sexually-transmitted infections. Physiology & Behavior, 41, 321–325.Google Scholar
Hethcote, H. & Yorke, J.A. (1984) Gonorrhea Transmission Dynamics and Control. Berlin: Springer-Verlag.Google Scholar
Hurst, G.D.D., Jiggins, F.M., Schulenburg, J.H.G.V.D., et al. (1999a) Male-killing Wolbachia in two species of insect. Proceedings of the Royal Society of London B, 266, 735–740.Google Scholar
Hurst, G.D.D., Sharpe, R.G., Broomfield, A.H., et al. (1995) Sexually transmitted disease in a promiscuous insect, Adalia bipunctata. Ecological Entomology, 20, 230–236.Google Scholar
Hurst, G.D.D., Von Der Schulenburg, J.H.G., Majerus, T.M.O., et al. (1999b) Invasion of one insect species, Adalia bipunctata, by two different male-killing bacteria. Insect Molecular Biology, 8, 133–139.Google Scholar
Jackson, M., White, N., Giffard, P. & Timms, P. (1999) Epizootiology of Chlamydia infections in two free-range koala populations. Veterinary Microbiology, 65, 225–234.CrossRefGoogle ScholarPubMed
Ji, W., White, P.C.L. & CLout, M.N. (2005) Contact rates between possums revealed by proximity data loggers. Journal of Applied Ecology, 42, 595–604.Google Scholar
Jones, S.L., Pastok, D. & Hurst, G.D.D. (2015) No evidence that presence of sexually transmitted infection selects for reduced mating rate in the two spot ladybird, Adalia bipunctata. Peer J, 3, e1148.Google Scholar
Keeling, M. (2005) The implications of network structure for epidemic dynamics. Theoretical Population Biology, 67, 1–8.CrossRefGoogle ScholarPubMed
Keeling, M.J. (1999) The effects of local spatial structure on epidemiological invasions. Proceedings of the Royal Society of London B, 266, 859–867.Google Scholar
Knell, R.J. (1999) Sexually transmitted disease and parasite mediated sexual selection. Evolution, 53, 957–961.Google Scholar
Knell, R.J. & Webberley, K.M. (2004) Sexually transmitted diseases of insects: distribution, ecology, evolution and host behaviour. Biological Reviews, 79, 557–581.Google Scholar
Kokko, H. & Rankin, D.J. (2006) Lonely hearts or sex in the city? Density-dependent effects in mating systems. Philosophical Transactions of the Royal Society of London B, 361, 319–334.Google Scholar
Kokko, H., Ranta, E., Ruxton, G. & Lundberg, P. (2002) Sexually transmitted disease and the evolution of mating systems. Evolution, 56, 1091–1100.Google Scholar
Kulkarni, S. & Heeb, P. 2007. Social and sexual behaviours aid transmission of bacteria in birds. Behavioural Processes, 74, 88–92.Google Scholar
Lockhart, A.B., Thrall, P.H. & Antonovics, J. (1996) Sexually transmitted diseases in animals: ecological and evolutionary implications. Biological Reviews, 71, 415–471.Google Scholar
Loehle, C. (1995) Social barriers to pathogen transmission in wild animal populations. Ecology, 76, 326–335.Google Scholar
Lombardo, M.P., Thorpe, P.A. & Power, H.W. (1999) The beneficial sexually transmitted microbe hypothesis of avian copulation. Behavioral Ecology, 10, 333–337.Google Scholar
Lunney, D., Crowther, M.S., Wallis, I., et al. (2012) Koalas and climate change: a case study on the Liverpool Plains, north-west New South Wales. In: Lunney, D. & Hutchings, P. (eds.), Wildlife and Climate Change: Towards Robust Conservation Strategies for Australian Fauna (pp. 150–168). Mosman, NSW: Royal Zoological Society of New South Wales.Google Scholar
Luong, L.T., Platzer, E.G., Zuk, M. & Giblin-Davis, R.M. (2000) Venereal worms: sexually transmitted nematodes in the decorated cricket. Journal of Parasitology, 86, 471–477.Google Scholar
May, R.M. & Anderson, R.M. (1979) Population biology of infectious diseases: Part II. Nature, 280, 455–461.Google Scholar
May, R.M. & Anderson, R.M. (1987) Transmission dynamics of HIV infection. Nature, 326, 137–142.Google Scholar
May, R.M., Gupta, S. & McLean, A.R. (2001) Infectious disease dynamics: what characterizes a successful invader? Philosophical Transactions of the Royal Society of London B, 356, 901–910.Google Scholar
McColl, K., Martin, R., Gleeson, L., Handasyde, K. & Lee, A. (1984) Chlamydia infection and infertility in the female koala (Phascolarctos cinereus). Veterinary Record, 115, 655–655.Google Scholar
Mitchell, P., Bilney, R. & Martin, R. (1988) Population-structure and reproductive status of koalas on Raymond Island, Victoria. Wildlife Research, 15, 511–514.Google Scholar
Moore, S.L. & Wilson, K. (2002) Parasites as a viability cost of sexual selection in natural populations of mammals. Science, 297, 2015–2018.Google Scholar
Morand, S. (1993) Sexual transmission of a nematode: study of a model. Oikos, 66, 48–54.Google Scholar
Morand, S. & Faliex, E. (1994) Study on the life cycle of a sexually transmitted nematode parasite of a terrestrial snail. Journal of Parasitology, 80, 1049–1052.Google Scholar
Nahrung, H.F. & Allen, G.R. (2004) Sexual selection under scramble competition: mate location and mate choice in the eucalypt leaf beetle Chrysophtharta agricola (Chapuis) in the field. Journal of Insect Behavior, 17, 353–366.CrossRefGoogle Scholar
Nahrung, H.F. & Clarke, A.R. (2007) Sexually-transmitted disease in a sub-tropical eucalypt beetle: infection of the fittest? Evolutionary Ecology, 21, 143–156.Google Scholar
Nunn, C.L. (2003) Behavioural defenses against sexually transmitted diseases in primates. Animal Behaviour, 66, 37–48.Google Scholar
Nunn, C.L. & Altizer, S. (2004) Sexual selection, behaviour and sexually transmitted diseases. In: Kappeler, P.M. & van Schaik, C.P. (eds.), Sexual Selection in Primates: New and Comparative Perspectives (pp. 117–130). Cambridge: Cambridge University Press.Google Scholar
Nunn, C.L., Scully, E.J., Kutsukake, N., et al. (2014) Mating competition, promiscuity, and life history traits as predictors of sexually transmitted disease risk in primates. International Journal of Primatology, 35, 764–786.Google Scholar
Otti, O., McTighe, A.P. & Reinhardt, K. (2013) In vitro antimicrobial sperm protection by an ejaculate-like substance. Functional Ecology, 27, 219–226.CrossRefGoogle Scholar
Pastok, D., Hoare, M.J., Ryder, J.J., et al. (2016) The role of host phenology in determining the incidence of an insect sexually transmitted infection. Oikos, 125, 636–643.Google Scholar
Peng, Y., Grassl, J., Millar, A.H. & Baer, B. (2016) Seminal fluid of honeybees contains multiple mechanisms to combat infections of the sexually transmitted pathogen Nosema apis. Proceedings of the Royal Society of London B, 283, 2015.1785.Google Scholar
Perry, J.C., Sharpe, D.M.T. & Rowe, L. (2009) Condition-dependent female remating resistance generates sexual selection on male size in a ladybird beetle. Animal Behaviour, 77, 743–748.Google Scholar
Poiani, A. & Wilks, C. (2000) Sexually transmitted diseases: a possible cost of promiscuity in birds? The Auk, 117, 1061–1065.Google Scholar
Poinar, G.O.J. (1970) Orycetonema genitalis gen. et sp. nov. (Rhabditidae: Nematoda) from the genital system of Orycetes monoceros L. (Scarabaeidae: Coleoptera) in West Africa. Journal of Helminthology, 44, 1–10.Google Scholar
Riddick, E.W. (2010) Ectoparasitic mite and fungus on an invasive lady beetle: parasite coexistence and influence on host survival. Bulletin of Insectology, 63, 13–20.Google Scholar
Rowe, L. (1992) Convenience polyandry in a water strider – foraging conflicts and female control of copulation frequency and guarding duration. Animal Behaviour, 44, 189–202.Google Scholar
Rushmore, J., Caillaud, D., Hall, R.J., et al. (2014) Network-based vaccination improves prospects for disease control in wild chimpanzees. Journal of the Royal Society Interface, 11(97), 20140349.Google Scholar
Rushmore, J., Caillaud, D., Matamba, L., et al. (2013) Social network analysis of wild chimpanzees provides insights for predicting infectious disease risk. Journal of Animal Ecology, 82, 976–986.Google Scholar
Ryder, J.J., Hoare, M.-J., Pastok, D., et al. (2014) Disease epidemiology in arthropods is altered by the presence of nonprotective symbionts. American Naturalist, 183, E89–E104.Google Scholar
Ryder, J.J., Miller, M.R., White, A., Knell, R.J. & Boots, M. (2007) Host–parasite population dynamics under combined frequency- and density-dependent transmission. Oikos, 116, 2017–2026.Google Scholar
Ryder, J.J., Pastok, D., Hoare, M.-J., et al. (2013) Spatial variation in food supply, mating behavior, and sexually transmitted disease epidemics. Behavioral Ecology, 24, 723–729.Google Scholar
Ryder, J.J., Webberley, K.M., Boots, M. & Knell, R.J. (2005) Measuring the transmission dynamics of a sexually transmitted disease. Proceedings of the National Academy of Sciences of the United States Of America, 102, 15,140–15,143.Google Scholar
Samakovlis, C., Kylsten, P., Kimbrell, D.A., Engström, A. & Hultmark, D. (1991) The Andropin gene and its product, a male-specific antibacterial peptide in Drosophila melanogaster. EMBO J, 10, 163–169.Google Scholar
Schmid-Hempel, P. (1998) Parasites of Social Insects, Princeton, NJ: Princeton University Press.Google Scholar
Seeman, O.D. & Nahrung, H.F. (2004) Female biased parasitism and the importance of host generation overlap in a sexually transmitted parasite of beetles. Journal of Parasitology, 90, 114–118.Google Scholar
Simmons, A.M. & Rogers, C.E. (1990) Distribution and prevalence of an ectoparasitic nematode, Noctuidonema guyanese, on moths of the fall armyworm (Lepidoptera: Noctuidae) in the tropical Americas. Journal of Entomological Science, 25, 510–518.Google Scholar
Simmons, A.M. & Rogers, C.E. (1994) Effects of an ectoparasitic nematode, Noctuidonema guyanese on adult longevity and egg fertility in Spodoptera frugiperda (Lepidoptera: Noctuidae). Biological Control, 4, 285–289.Google Scholar
Smith, C.C. & Mueller, U.G. (2015) Sexual transmission of beneficial microbes. Trends in Ecology & Evolution, 30, 438–440.Google Scholar
Stalder, K., Vaz, P.K., Gilkerson, J.R., et al. (2015) Prevalence and clinical significance of Herpesvirus infection in populations of Australian marsupials. PLoS ONE, 10.Google Scholar
Suganuma, K., Narantsatsral, S., Battur, B., et al. (2016) Isolation, cultivation and molecular characterization of a new Trypanosoma equiperdum strain in Mongolia. Parasites & Vectors, 9, 481.Google Scholar
Sugimoto, C., Isayama, Y., Sakazaki, R. & Kuramochi, S. (1983) Transfer of Hemophilus equigenitalis Taylor et al. 1978 to the genus Taylorella gen-nov as Taylorella equigenitalis comb. nov. Current Microbiology, 9, 155–162.Google Scholar
Telfer, S., Lambin, X., Birtles, R., et al. (2010) Species interactions in a parasite community drive infection risk in a wildlife population. Science, 330, 243–246.Google Scholar
Waterman, J.M. (2010) The adaptive function of masturbation in a promiscuous African ground squirrel. PLoS ONE, 5, e13060.Google Scholar
Webberley, K.M., Buszko, J., Isham, V. & Hurst, G.D.D. (2006a) Sexually transmitted disease epidemics in a natural insect population. Journal of Animal Ecology, 75, 33–43.Google Scholar
Webberley, K.M. & Hurst, G.D.D. (2002) The effect of aggregative overwintering on an insect sexually transmitted parasite system. Journal of Parasitology, 88, 707–712.Google Scholar
Webberley, K.M., Hurst, G.D.D., Buszko, J. & Majerus, M.E.N. (2002) Lack of parasite-mediated sexual selection in a ladybird/sexually transmitted disease system. Animal Behaviour, 63, 131–141.Google Scholar
Webberley, K.M., Hurst, G.D.D., Husband, R.W., et al. (2004) Host reproduction and a sexually transmitted disease: causes and consequences of Coccipolipus hippodamiae distribution on coccinellid beetles. Journal of Animal Ecology, 73, 1–10.Google Scholar
Webberley, K.M., Tinsley, M.C., Sloggett, J.J., Majerus, M.E.N. & Hurst, G.D.D. (2006b) Spatial variation in the incidence of a sexually transmitted parasite of the ladybird beetle Adalia bipunctata (Coleoptera: Coccinellidae). European Journal of Entomology, 103, 793–797.CrossRefGoogle Scholar
Weigler, B.J., Girjes, A.A., White, N.A., et al. (1988) Aspects of the epidemiology of Chlamydia psittaci infection in a population of koalas (Phascolarctos cinereus) in southeastern Queensland, Australia. Journal of Wildlife Diseases, 24, 282–291.Google Scholar
Welch, V.L., Sloggett, J.J., Webberley, K.M. & Hurst, G.D.D. (2001) Short-range clinal variation in the prevalence of a sexually transmitted fungus associated with urbanisation. Ecological Entomology, 26, 547–550.Google Scholar
Werren, J.H., Hurst, G.D.D., Zhang, W., et al. (1994) Rickettsial relative associated with male killing in the ladybird beetle (Adalia bipunctata). Journal of Bacteriology, 176, 388–394.Google Scholar
White, J., Richard, M., Massot, M. & Meylan, S. (2011) Cloacal bacterial diversity increases with multiple mates: evidence of sexual transmission in female common lizards. PLoS ONE, 6, e22339.Google Scholar
White, N. & Timms, P. (1994) Chlamydia psittaci in a koala (Phascolarctos cinereus) population in south-east Queensland. Wildlife Research, 21, 41–47.Google Scholar
Xiang, J., Wünschmann, S., Diekema, D.J., et al. (2001) Effect of coinfection with GB virus C on survival among patients with HIV infection. New England Journal of Medicine, 345, 707–714.Google Scholar
Yorke, J.A., Hethcote, H.W. & Nold, A. (1978) Dynamics and control of the transmission of gonnorhea. Sexually Transmitted Diseases, 5, 51–56.Google Scholar

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