Abstract
Elucidating the factors determining reproductive success has challenged scientists since Darwin, but the exact pathways that shape the evolution of life history traits by connecting extrinsic (e.g., landscape structure) and intrinsic (e.g., female’s age and endosymbionts) factors and reproductive success have rarely been studied. Here we collected female fleas from wild rodents in plots differing in their densities and proportions of the most dominant rodent species. We then combined path analysis and model selection approaches to explore the network of effects, ranging from micro to macroscales, determining the reproductive success of these fleas. Our results suggest that female reproductive success is directly and positively associated with their infection by Mycoplasma bacteria and their own body mass, and with the rodent species size and total density. In addition, we found evidence for indirect effects of rodent sex and rodent community diversity on female reproductive success. These results highlight the importance of exploring interrelated factors across organization scales while studying the reproductive success of wild organisms, and they have implications for the control of vector-borne diseases.
Similar content being viewed by others
References
Baker JA, Heins DC, Foster SA, King RW (2008) An overview of life-history variation in female three-spine stickleback. Behaviour 145:579–602. doi:10.1163/156853908792451539
Balashov YS (1984) Interaction between blood sucking arthropods and their hosts, and its influence on vector potential. Annu Rev Entomol 29:137–156
Bashey F (2006) Cross-generational environmental effects and the evolution of offspring size in the Trinidadian guppy Poecilia reticulata. Evolution 60:348–361. doi:10.1554/05-087.1
Begon M et al (1999) Transmission dynamics of a zoonotic pathogen within and between wildlife host species. Proc R Soc Lond B 266:1939–1945
Bezemer TM, Harvey JA, Mills NJ (2005) Influence of adult nutrition on the relationship between body size and reproductive parameters in a parasitoid wasp. Ecol Entomol 30:571–580. doi:10.1111/j.0307-6946.2005.00726.x
Booksmythe I, Mautz B, Davis J, Nakagawa S, Jennions MD (2017) Facultative adjustment of the offspring sex ratio and male attractiveness: a systematic review and meta-analysis. Biol Rev 92:108–134. doi:10.1111/brv.12220
Bosch J, Vicens N (2006) Relationship between body size, provisioning rate, longevity and reproductive success in females of the solitary bee Osmia cornuta. Behav Ecol Sociobiol 60:26–33. doi:10.1007/s00265-005-0134-4
Brady CJ, Noske RA (2006) Generalised regressions provide good estimates of insect and spider biomass in the monsoonal tropics of Australia. Aust J Entomol 45:187–191. doi:10.1111/j.1440-6055.2006.00533.x
Burnham KP, Anderson DR (2002) Model selection and multimodel inference. A practical information-theoretic approach, 2nd edn. Springer, New York
Burt A, Trivers R (2006) Genes in conflict: the biology of selfish genetic elements. Harvard University, Cambridge
Calvitti M, Marini F, Desiderio A, Puggioli A, Moretti R (2015) Wolbachia density and cytoplasmic incompatibility in Aedes albopictus: concerns with using artificial Wolbachia infection as a vector suppression tool. PLoS One 10. doi:10.1371/journal.pone.0121813 (ARTN e0121813)
Carriere Y, Roff DA (1995) The evolution of offspring size and number: a test of the Smith-Fretwell model in three species of crickets. Oecologia 102:389–396. doi:10.1007/Bf00329806
Chomel BB et al (1996) Experimental transmission of Bartonella henselae by the cat flea. J Clin Microbiol 34:1952–1956
Clutton-Brock TH (1988) Reproductive success. In: Clutton-Brock TH (ed) Reproductive success: studies of individual variation in contrasting breeding systems, vol 29. University of Chicago, Chicago
Cohen C, Einav M, Hawlena H (2015a) Path analyses of cross-sectional and longitudinal data suggest that variability in natural communities of blood-associated parasites is derived from host characteristics and not interspecific interactions. Parasit Vector 8:429. doi:10.1186/S13071-015-1029-5
Cohen C, Toh E, Munro D, Dong Q, Hawlena H (2015b) Similarities and seasonal variations in bacterial communities from the blood of rodents and from their flea vectors. ISME J 9:1662–1676
Degen AA, Kam M (1991) Average daily metabolic-rate of gerbils of two species—Gerbillus pyramidum and Gerbillus allenbyi. J Zool 223:143–149
Dickerson BR, Brinck KW, Willson MF, Bentzen P, Quinn TP (2005) Relative importance of salmon body size and arrival time at breeding grounds to reproductive success. Ecology 86:347–352. doi:10.1890/03-625
Donelson JM, McCormick MI, Munday PL (2008) Parental condition affects early life-history of a coral reef fish. J Exp Mar Biol Ecol 360:109–116. doi:10.1016/j.jembe.2008.04.007
Edgerly JS, Livdahl TP (1992) Density-dependent interactions within a complex life-cycle: the roles of cohort structure and mode of recruitment. J Anim Ecol 61:139–150. doi:10.2307/5517
Ellegren H, Sheldon BC (2008) Genetic basis of fitness differences in natural populations. Nature 452:169–175. doi:10.1038/nature06737
Ellers J, Driessen G, Sevenster JG (2000) The shape of the trade-off function between egg production and life span in the parasitoid Asobara tabida. Neth J Zool 50:29–36. doi:10.1163/156854200505784
Ewald PW (1983) Host-parasite relations, vectors, and the evolution of disease severity. Annu Rev Ecol Syst 14:465–485
Fincke OM (1988) Sources of variation in lifetime reproductive success in a nonterritorial damselfly (Odonata: Coenagrionidae). In: Clutton-Brock TH (ed) Reproductive success: studies of individual variation in contrasting breeding systems, vol 3. University of Chicago, Chicago
Fischer B, Taborsky B, Kokko H (2011) How to balance the offspring quality-quantity tradeoff when environmental cues are unreliable. Oikos 120:258–270. doi:10.1111/j.1600-0706.2010.18642.x
Fox CW, Czesak ME (2000) Evolutionary ecology of progeny size in arthropods. Annu Rev Entomol 45:341–369. doi:10.1146/annurev.ento.45.1.341
Ganihar SR (1997) Biomass estimates of terrestrial arthropods based on body length. J Biosci 22:219–224. doi:10.1007/Bf02704734
Gavish Y et al (2014) Association of host and microbial species diversity across spatial scales in desert rodent communities. PLoS One 9:e109677. doi:10.1371/journal.pone.0109677
Gillespie SH, Smith GL, Osbourn AE (2004) Microbe-vector interactions in vector-borne diseases: sixty-third symposium of the society for general microbiology held at the University of Bath March 2004. Cambridge University, Cambridge
Gutiérrez R, Morick D, Cohen C, Hawlena H, Harrus S (2014) The effect of ecological and temporal factors on the composition of Bartonella infection in rodents and their fleas. ISME J 8:1598–1608. doi:10.1038/ismej.2014.22
Hawlena H, Abramsky Z, Krasnov BR (2005) Age-biased parasitism and density-dependent distribution of fleas (Siphonaptera) on a desert rodent. Oecologia 146:200–208. doi:10.1007/s00442-005-0187-0
Hawlena H, Abramsky Z, Krasnov BR (2006a) Ectoparasites and age-dependent survival in a desert rodent. Oecologia 148:30–39. doi:10.1007/s00442-005-0345-4
Hawlena H, Khokhlova IS, Abramsky Z, Krasnov BR (2006b) Age, intensity of infestation by flea parasites and body mass loss in a rodent host. Parasitology 133:187–193
Hawlena H, Abramsky Z, Krasnov BR (2007a) Ultimate mechanisms of age-biased flea parasitism. Oecologia 154:601–609
Hawlena H, Abramsky Z, Krasnov BR, Saltz D (2007b) Host defence versus intraspecific competition in the regulation of infrapopulations of the flea Xenopsylla conformis on its rodent host Meriones crassus. Int J Parasitol 37:919–925. doi:10.1016/j.ijpara.2007.01.015
Hawlena H et al (2013) The arthropod, but not the vertebrate host or its environment, dictates bacterial community composition of fleas and ticks. ISME J 7:221–223. doi:10.1038/ismej.2012.71
Herreras MV, Montero FE, Marcogliese DJ, Raga JA, Balbuena JA (2007) Phenotypic tradeoffs between egg number and egg size in three parasitic anisakid nematodes. Oikos 116:1737–1747. doi:10.1111/j.2007.0030-1299.16016.x
Hódar JA (1997) The use of regression equations for the estimation of prey length and biomass in diet studies of insectivore vertebrates. Miscel lània Zoològica 20:1–10
Honek A (1993) Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos 66:483–492. doi:10.2307/3544943
Horn DJ, Phillips ML, Koford RR, Clark WR, Sovada MA, Greenwood RJ (2005) Landscape composition, patch size, and distance to edges: interactions affecting duck reproductive success. Ecol Appl 15:1367–1376. doi:10.1890/03-5254
Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108
Johnson PTJ, Preston DL, Hoverman JT, Richgels KLD (2013) Biodiversity decreases disease through predictable changes in host community competence. Nature 494:230–233
Jorgensen C, Auer SK, Reznick DN (2011) A model for optimal offspring size in fish, including live-bearing and parental effects. Am Nat 177:E119–E135. doi:10.1086/659622
Kedem H, Cohen C, Messika I, Einav M, Pilosof S, Hawlena H (2014) Multiple effects of host species diversity on co-existing host-specific and host-opportunistic microbes. Ecology 95:1173–1183. doi:10.1890/13-0678.1
Khokhlova IS, Krasnov BR, Shenbrot GI, Degen AA (1994) patterns affecting seasonal body mass change in several species of rodents in the Ramon erosion cirque, Negev Highlands, Israel (in Russian with English summary). Zool Zhur 73:106–114
Khokhlova I, Krasnov BR, Shenbrot GI, Degen AA (2001) Body mass and environment: a study in Negev rodents. Isr J Zool 47:1–13
Khokhlova IS, Fielden LJ, Williams JB, Degen AA, Krasnov BR (2013) Energy expenditure for egg production in arthropod ectoparasites: the effect of host species. Parasitology 140:1070–1077. doi:10.1017/S0031182013000449
Khokhlova IS, Pilosof S, Fielden LJ, Degen AA, Krasnov BR (2014) A trade-off between quantity and quality of offspring in haematophagous ectoparasites: the effect of the level of specialization. J Anim Ecol 83:397–405. doi:10.1111/1365-2656.12134
Krasnov BR (2008) Functional and evolutionary ecology of fleas: a model for ecological parasitology. Cambridge University, Cambridge
Krasnov B, Khokhlova I, Shenbrot G (2002a) The effect of host density on ectoparasite distribution: an example of a rodent parasitized by fleas. Ecology 83:164–175
Krasnov BR, Khokhlova IS, Oguzoglu I, Burdelova NV (2002b) Host discrimination by two desert fleas using an odour cue. Anim Behav 64:33–40
Krasnov BR, Burdelova NV, Khokhlova IS, Shenbrot GI, Degen A (2005a) Larval interspecific competition in two flea species parasitic on the same rodent host. Ecol Entomol 30:146–155
Krasnov BR, Khokhlova IS, Arakelyan MS, Degen AA (2005b) Is a starving host tastier? Reproduction in fleas parasitizing food-limited rodents. Funct Ecol 19:625–631
Krasnov BR, Morand S, Hawlena H, Khokhlova IS, Shenbrot GI (2005c) Sex-biased parasitism, seasonality and sexual size dimorphism in desert rodents. Oecologia 146:209–217. doi:10.1007/s00442-005-0189-y
Krasnov BR, Shenbrot GI, Khokhlova IS, Hawlena H, Degen AA (2006) Temporal variation in parasite infestation of a host individual: does a parasite-free host remain uninfested permanently? Parasitol Res 99:541–545
Krebs CJ, Keller BL, Tamarin RH (1969) Microtus population biology: demographic changes in fluctuating populations of M. ochrogaster and M. pennsylvanicus in southern Indiana. Ecology 50:587–607
Kudo S (2001) Intraclutch egg-size variation in acanthosomatid bugs: adaptive allocation of maternal investment? Oikos 92:208–214. doi:10.1034/j.1600-0706.2001.920202.x
Lajeunesse MJ, Forbes MR (2002) Host range and local parasite adaptation. Proc R Soc B 269:703–710
Lefevre T, Thomas F (2008) Behind the scene, something else is pulling the strings: emphasizing parasitic manipulation in vector-borne diseases. Infect Genet Evol 8:504–519. doi:10.1016/j.meegid.2007.05.008
Lim JN, Senior AM, Nakagawa S (2014) Heterogeneity in individual quality and reproductive trade-offs within species. Evolution 68:2306–2318. doi:10.1111/evo.12446
Lindstrom J (1999) Early development and fitness in birds and mammals. Trends Ecol Evol 14:343–348. doi:10.1016/S0169-5347(99)01639-0
Loot G, Poulet N, Brosse S, Tudesque L, Thomas F, Blanchet S (2011) Determinants of life-history traits in a fish ectoparasite: a hierarchical analysis. Parasitology 138:848–857. doi:10.1017/S003118201100014x
Ma LM (2000) Body length of fleas in relation to some factors, and influence of host nutrition on fleas. Acta Parasitologica et Medica Entomologica Sinica 7:235–240
Major RE, Kendal CE (1996) The contribution of artificial nest experiments to understanding avian reproductive success: a review of methods and conclusions. Ibis 138:298–307. doi:10.1111/j.1474-919X.1996.tb04342.x
Marshall DJ, Cook CN, Emlet RB (2006) Offspring size effects mediate competitive interactions in a colonial marine invertebrate. Ecology 87:214–225. doi:10.1890/05-0350
Martin CA, Proulx R, Magnan P (2014) The biogeography of insects length-dry mass relationships. Insect Conserv Diver 7:413–419. doi:10.1111/icad.12063
Moller AP (1997) Developmental stability and fitness: a review. Am Nat 149:916–932
Morick D, Krasnov BR, Khokhlova IS, Gottlieb Y, Harrus S (2011) Investigation of Bartonella acquisition and transmission in Xenopsylla ramesis fleas (Siphonaptera: Pulicidae). Mol Ecol 20:2864–2870. doi:10.1111/j.1365-294X.2011.05033.x
Morick D, Krasnov BR, Khokhlova IS, Gottlieb Y, Harrus S (2013a) Transmission dynamics of Bartonella sp strain OE 1-1 in Sundevall’s Jirds (Meriones crassus). Appl Environ Microbiol 79:1258–1264. doi:10.1128/Aem.03011-12
Morick D et al (2013b) Effects of Bartonella spp. on flea feeding and reproductive performance. Appl Environ Microbiol 79:3438–3443
Muthén LK, Muthén BO (2012) Mplus user’s guide: statistical analysis with latent variables. Muthén & Muthén, Los Angeles
Olofsson H, Ripa J, Jonzen N (2009) Bet-hedging as an evolutionary game: the trade-off between egg size and number. Proc R Soc B 276:2963–2969. doi:10.1098/rspb.2009.0500
Palmer AR, Strobeck C (2003) Fluctuating asymmetry analyses revisited. In: Polak M (ed) Developmental instability: causes and consequences, vol 17. Oxford University, Oxford
Parker GA, Begon M (1986) Optimal egg size and clutch size: effects of environment and maternal phenotype. Am Nat 128:573–592. doi:10.1086/284589
Pedhazur EJ (1983) Multiple-Regression in behavioral-research: explanation and prediction, 2nd edn. Harcourt Brace, Orlando
Peig J, Green AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118:1883–1891. doi:10.1111/j.1600-0706.2009.17643.x
R-Core-Team (2013) R: a language and environment for statistical computing foundation for statistical computing. Austria, Vienna
Reznick D, Nunney L, Tessier A (2000) Big houses, big cars, superfleas and the costs of reproduction. Trends Ecol Evol 15:421–425. doi:10.1016/S0169-5347(00)01941-8
Roff DA (1992) The evolution of life histories: theory and analysis. Chapman & Hall, New York
Roff DA (2002) Life history evolution. Sinauer, Sunderland
Rollinson N, Hutchings JA (2013) Environmental quality predicts optimal egg size in the wild. Am Nat 182:76–90. doi:10.1086/670648
Rosenberg E, Zilber-Rosenberg I (2011) Symbiosis and development: the hologenome concept. Birth Defects Res C 93:56–66. doi:10.1002/bdrc.20196
Rosenfeld CS, Roberts RM (2004) Maternal diet and other factors affecting offspring sex ratio: a review. Biol Reprod 71:1063–1070. doi:10.1095/biolreprod.104.030890
Rosenheim JA, Alon U, Shinar G (2010) Evolutionary balancing of fitness limiting factors. Am Nat 175:662–674. doi:10.1086/652468
Saccheri I, Hanski I (2006) Natural selection and population dynamics. Trends Ecol Evol 21:341–347. doi:10.1016/j.tree.2006.03.018
Salkeld DJ, Padgett KA, Jones JH (2013) A meta-analysis suggesting that the relationship between biodiversity and risk of zoonotic pathogen transmission is idiosyncratic. Ecol Lett 16:679–686
Sargent RD, Reid ML (1999) Unexpected offspring sex ratios in response to habitat quality in a size-dimorphic Bark beetle. Can J Zool 77:524–529. doi:10.1139/Cjz-77-4-524
Schoener TW (1980) Length-weight regressions in tropical and temperate forest-understory insects. Ann Entomol Soc Am 73:106–109
Segoli M, Rosenheim JA (2013) The link between host density and egg production in a parasitoid insect: comparison between agricultural and natural habitats. Funct Ecol 27:1224–1232. doi:10.1111/1365-2435.12109
Segoli M, Hoffmann AA, Lloyd J, Omodei GJ, Ritchie SA (2014) The effect of virus-blocking Wolbachia on male competitiveness of the dengue vector mosquito Aedes aegypti. PLoS Negl Trop Dis 8:e3294. doi:10.1371/journal.pntd.0003294
Seidelmann K, Ulbrich K, Mielenz N (2010) Conditional sex allocation in the red mason bee, Osmia rufa. Behav Ecol Sociobiol 64:337–347. doi:10.1007/s00265-009-0850-2
Seppala O, Liljeroos K, Karvonen A, Jokela J (2008) Host condition as a constraint for parasite reproduction. Oikos 117:749–753. doi:10.1111/j.0030-1299.2008.16396.x
Sisterson MS (2009) Transmission of insect-vectored pathogens: effects of vector fitness as a function of infectivity status. Environ Entomol 38:345–355
Stearns SC (1992) The evolution of life histories. Oxford University, Oxford
Tepedino VJ, Torchio PF (1982) Phenotypic variability in nesting success among Osmia lignaria propinqua females in a glasshouse environment: (Hymenoptera: Megachilidae). Ecol Entomol 7:453–462. doi:10.1111/j.1365-2311.1982.tb00688.x
Tripet F, Jacot A, Richner H (2002) Larval competition affects the life histories and dispersal behavior of an avian ectoparasite. Ecology 83:935–945
Trivers RL, Willard DE (1973) Natural selection of parental ability to vary sex ratio of offspring. Science 179:90–92. doi:10.1126/science.179.4068.90
Tsai ML, Li JJ, Dai CF (2001) How host size may constrain the evolution of parasite body size and clutch size. The parasitic isopod Ichthyoxenus fushanensis and its host fish, Varicorhinus bacbatulus, as an example. Oikos 92:13–19. doi:10.1034/j.1600-0706.2001.920102.x
Tschirren B, Bischoff LL, Saladin V, Richner H (2007) Host condition and host immunity affect parasite fitness in a bird-ectoparasite system. Funct Ecol 21:372–378
Wagner CE, Harmon LJ, Seehausen O (2014) Cichlid species-area relationships are shaped by adaptive radiations that scale with area. Ecol Lett 17:583–592. doi:10.1111/ele.12260
Werner EE, Anholt BR (1993) Ecological consequences of the trade-off between growth and mortality-rates mediated by foraging activity. Am Nat 142:242–272. doi:10.1086/285537
Wilson AJ, Pemberton JM, Pilkington JG, Clutton-Brock TH, Kruuk LEB (2009) Trading offspring size for number in a variable environment: selection on reproductive investment in female Soay sheep. J Anim Ecol 78:354–364. doi:10.1111/j.1365-2656.2008.01489.x
Wood CL, Lafferty KD, DeLeo G, Young HS, Hudson PJ, Kuris AM (2014) Does biodiversity protect humans against infectious disease? Ecology 95:817–832. doi:10.1890/13-1041.1
Woods JE, Brewer MM, Hawley JR, Wisnewski N, Lappin MR (2005) Evaluation of experimental transmission of ‘Candidatus Mycoplasma haemominutum’ and Mycoplasma haemofelis by Ctenocephalides felis to cats. Am J Vet Res 66:1008–1012
Woods JE, Wisnewski N, Lappin MR (2006) Attempted transmission of ‘Candidatus Mycoplasma haemominutum’ and Mycoplasma haemofelis by feeding cats infected Ctenocephalides felis. Am J Vet Res 67:494–497
Woog F (2002) Reproductive success and pairing in Hawaiian Geese (Branta sandvicensis) in relation to age and body size. J Ornithol 143:43–50. doi:10.1007/bf02465457
Wootton JT (1994) Predicting direct and indirect effects: an integrated approach using experiments and path analysis. Ecology 75:151–165. doi:10.2307/1939391
Yuval B, Ben-Ami E, Behar A, Ben-Yosef M, Jurkevitch E (2013) The Mediterranean fruit fly and its bacteria: potential for improving sterile insect technique operations. J Appl Entomol 137:39–42
Zindel R, Gottlieb Y, Aebi A (2011) Arthropod symbioses: a neglected parameter in pest- and disease-control programmes. J Appl Ecol 48:864–872. doi:10.1111/j.1365-2664.2011.01984.x
Acknowledgements
We thank M. Einav, Z. Sigal, E. Hyams, A. Novoplansky, M. Segoli, and A. Tsairi for valuable advice during this study. We are grateful to D.A. Apansakevich and N. Burdelova for the flea and tick taxonomic identifications. This study was supported by the Israel Science Foundation (ISF), Grant Number 1391/15 and by the Marie Curie Career Integration Grant (CIG) number FP7-293713 to H.H. and by the United States–Israel Binational Science Foundation, grant number 2012063 to H.H. (PI), K. Clay, C. Fuqua and Q. Dong. M.G. was sponsored by The Kreitman School of Advanced Graduate Studies (Ben-Gurion University of the Negev) and the Blaustein Center for Scientific Cooperation (Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev). This is publication number 939 of the Mitrani Department of Desert Ecology. The trapping and handling protocol was approved by the Ben-Gurion University Committee for the Ethical Care and Use of Animals in Experiments (permission # IL-14-03-2011) and by the Israel Nature and National Parks Protection Authority (permission # 2011/38146).
Author contribution statement
IM, HK, KC, CF, QD and HH conceived and designed the study. IM and HK performed the study. IM, MG, YG, and VC analyzed the data. IM, MG and HH wrote the manuscript; other authors provided editorial advice.
Data accessibility
Raw data and statistical scripts can be accessed via the public archive “Figshare.com”. Accession addresses are http://dx.doi.org/10.6084/m9.figshare.4818121 and http://dx.doi.org/10.6084/m9.figshare.4818136, respectively.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by George Heimpel.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Messika, I., Garrido, M., Kedem, H. et al. From endosymbionts to host communities: factors determining the reproductive success of arthropod vectors. Oecologia 184, 859–871 (2017). https://doi.org/10.1007/s00442-017-3906-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-017-3906-4