Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Does investment into “expensive” tissue compromise anti-parasitic defence? Testes size, brain size and parasite diversity in rodent hosts

Abstract

Species richness of parasite assemblages varies among host species. Earlier studies that searched for host-related determinants of parasite diversity mainly considered host traits that affect the probability of host encounter with parasites, whereas host traits related to defensibility against parasites have rarely been investigated. From the latter perspective, evolutionary investment in “expensive” tissue or organs (like testes or brain) may trade off against energetically costly anti-parasitic defences. If so, richer parasite assemblages are expected in hosts with larger testes and brains. We studied the relationships between testes and brain size and diversity of parasites (fleas, gamasid mites and helminths) in 55 rodent species using a comparative approach and application of two methods, namely the method of independent contrasts and generalized least-squares (GLS) analysis. Both phylogenetically correct methods produced similar results for flea and helminth species richness. Testes size positively correlated with flea and helminth species richness but not gamasid mite species richness. No correlation between brain size and species richness of any parasite group was found by the method of independent contrasts. However, GLS analysis indicated negative correlation between brain size and mite species richness. Our results cast doubt on the validity of the expensive tissue hypothesis, but suggest instead that larger testes are associated with higher parasite diversity via their effect on mobility and/or testosterone-mediated immunosuppression.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2

References

  1. Aiello LC, Wheeler P (1995) The expensive-tissue hypothesis: the brain and the digestive system in human and primate evolution. Curr Anthropol 36:199–221

  2. Alzaga V, Vicente J, Villanua D, Acevedo P, Casas F, Gortazar C (2008) Body condition and parasite intensity correlates with escape capacity in Iberian hares. Behav Ecol Sociobiol 62:769–775

  3. Arneberg P (2002) Host population density and body mass as determinants of species richness in parasites communities: comparative analyses of directly transmitted nematodes of mammals. Ecography 25:88–94

  4. Arrierero E, Møller AP (2008) Host ecology and life-history traits associated with blood parasite species richness in birds. J Evol Biol 21:1504–1513

  5. Bininda-Emonds ORP, Cardillo M, Jones KE, MacPhee RDE, Beck RMD, Grenyer R, Price SA, Vos RA, Gittleman JL, Purvis A (2007) The delayed rise of present-day mammals. Nature 446:507–512

  6. Bordes F, Morand S (2008) Helminth species diversity of mammals: parasite species richness is a host species attribute. Parasitology 135:1701–1705

  7. Bordes F, Morand S (2009a) Parasite diversity: an overlooked metric of parasite pressures? Oikos 118:801–806

  8. Bordes F, Morand S (2009b) Coevolution between multiple helminth infestations and basal immune investment in mammals: cumulative effects of polyparasitism? Parasitol Res 106:33–37

  9. Bordes F, Blumstein DT, Morand S (2007) Rodent sociality and parasite diversity. Biol Lett 3:692–694

  10. Bordes F, Morand S, Guerrero R (2008) Bat fly species richness in Neotropical bats: correlations with host ecology and host brain. Oecologia 158:109–116

  11. Bordes F, Morand S, Kelt DA, Van Vuren DH (2009) Home range and parasite diversity in mammals. Am Nat 173:467–474

  12. Breed WG, Taylor J (2000) Body mass, testes mass, and sperm size in murine rodents. J Mammal 81:758–768

  13. Combes C (2001) Parasitism. The ecology and evolution of intimate interactions. University of Chicago Press, Chicago

  14. Dechmann DKN, Safi K (2009) Comparative studies of brain evolution: a critical insight from the Chiroptera. Biol Rev 84:161–172

  15. Devevey G, Niculita-Herzel H, Biollaz F, Yvon C, Chapuisat M, Christe P (2008) Developmental, metabolic and immunological cost of flea infestation in the common vole. Funct Ecol 22:1091–1098

  16. Devillard S, Allainé D, Gaillard J-M, Pontier D (2004) Does social complexity lead to sex-biased dispersal in polygynous mammals? A test on ground-dwelling sciurids. Behav Ecol 15:83–87

  17. Eisenberg JF, Wilson DE (1978) Relative brain size and feeding strategies in the Chiroptera. Evolution 32:740–751

  18. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15

  19. Ferrari N, Cattadori IM, Nespereira J, Rizzoli A, Hudson PJ (2004) The role of host sex in parasite dynamics: field experiments on the yellow-necked mouse Apodemus flavicollis. Ecol Lett 7:88–94

  20. Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622

  21. Freckleton RP, Harvey PH, Pagel M (2002) Phylogenetic analysis and comparative data: a test and review of the evidence. Am Nat 160:712–726

  22. Gage MJG, Freckleton RP (2003) Relative testis size and sperm morphometry across mammals: no evidence for an association between sperm competition and sperm length. Proc R Soc Lond B 270:232–265

  23. Garland T, Díaz-Uriarte R (1999) Polytomies and phylogenetically independent contrasts: examination of the bounded degrees of freedom approach. Syst Biol 48:547–558

  24. Garland T, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Am Nat 41:18–32

  25. Garland T, Dickerman AWC, Janis M, Jones JA (1993) Phylogenetic analysis of covariance by computer simulation. Syst Biol 42:265–292

  26. Giorgi MS, Arlettaz R, Christe P, Vogel P (2001) The energetic grooming costs imposed by a parasitic mite (Spinturix myoti) upon its bat host (Myotis myotis). Proc R Soc Lond B 268:2071–2075

  27. Goüy de Bellocq J, Charbonnel N, Morand S (2008) Coevolutionary relationship between helminth diversity and MHC class II polymorphism in rodents. J Evol Biol 21:1144–1150

  28. Grear DA, Perkins SE, Hudson PJ (2009) Does elevated testosterone result in increased exposure and transmission of parasites? Ecol Lett 12:528–537

  29. Gromov IM, Polyakov IY (1992) Voles (Microtinae) (Fauna of the USSR. Mammals). Brill, Leiden

  30. Hafner MS, Hafner JC (1984) Brain size, adaptation and heterochrony in geomyoid rodents. Evolution 38:1088–1098

  31. Hanssen SA, Hasselquist D, Folstad I, Erikstad KE (2004) Costs of immunity: immune responsiveness reduces survival in a vertebrate. Proc R Soc Lond B 271:925–930

  32. Harcourt H, Harvey PH, Larson G, Short RV (1981) Testis weight, body weight and breeding system in primates. Nature 293:55–57

  33. Harvey PH, Pagel M (1991) The comparative method in evolutionary biology. Oxford University Press, Oxford

  34. Hawlena H, Bashary D, Abramsky Z, Krasnov BR (2007) Benefits, costs and constraints of anti-parasitic grooming in adult and juvenile rodents. Ethology 113:394–402

  35. Hladik CM, Chivers DJ, Pasquet P (1999) On diet and gut size in non-human primates and humans: is there a relationship to brain size? Curr Anthropol 40:695–697

  36. Hughes J, Page RDM (2007) Comparative tests of ectoparasite species richness in seabirds. BMC Evol Biol 7:227–248

  37. Hughes VL, Randolph SE (2001) Testosterone depresses innate and acquired resistance to ticks in natural rodent hosts: a force for aggregated distributions of parasites. J Parasitol 87:49–54

  38. Isler K, van Schaik C (2006) Costs of encephalization: the energy trade-off hypothesis tested on birds. J Human Evol 51:228–243

  39. Jacobs LF, Gaulin SJC, Sherry DF, Hoffman GE (1990) Evolution of spatial cognition: sex-specific patterns of spatial-behavior predict hippocampal size. Proc Natl Acad Sci USA 87:6349–6352

  40. Jokela J, Schmid-Hempel P, Rigby MC (2000) Dr. Pangloss restrained by the Red Quinn—steps towards a unified defence theory. Oikos 89:267–274

  41. Jones CJ (1996) Immune responses to fleas, bugs and sucking lice. In: Wikel SK (ed) The immunology of host-ectoparasitic arthropod relationships. CABI, Wallingford, pp 150-174

  42. Jones KE, MacLarnon AM (2004) Affording large brains: testing hypotheses of mammalian brain evolution in bats. Am Nat 164:20–31

  43. Kenagy GJ, Trombulak SC (1986) Size and function of mammalian testes in relation to body size. J Mamm 67:1–22

  44. Khokhlova IS, Spinu M, Krasnov BR, Degen AA (2004) Immune responses to fleas in two rodent species differing in natural prevalence of infestation and diversity of flea assemblages. Parasitol Res 94:304–311

  45. Korallo NP, Vinarski MV, Krasnov BR, Shenbrot GI, Mouillot D, Poulin R (2007) Are there general rules governing parasite diversity? Small mammalian hosts and gamasid mite assemblages. Divers Distrib 13:353–360

  46. Krasnov BR, Shenbrot GI, Khokhlova IS, Degen AA (2004) Flea species richness and parameters of host body, host geography and host “milieu”. J Anim Ecol 73:1121–1128

  47. Krasnov BR, Shenbrot GI, Mouillot D, Khokhlova IS, Poulin R (2005a) Spatial variation in species diversity and composition of flea assemblages in small mammalian hosts: geographic distance or faunal similarity? J Biogeogr 32:633–644

  48. Krasnov BR, Morand S, Hawlena H, Khokhlova IS, Shenbrot GI (2005b) Sex-biased parasitism, seasonality and sexual size dimorphism in desert rodents. Oecologia 146:209–217

  49. Krasnov BR, Korallo-Vinarskaya NP, Vinarski MV, Shenbrot GI, Mouillot D, Poulin R (2008) Searching for general patterns in parasite ecology: host identity vs. environmental influence on gamasid mite assemblages in small mammals. Parasitology 135:229–242

  50. Lello J, Boag B, Hudson PJ (2005) The effects of single and concomitant infections on condition and fecundity of the wild rabbits (Oryctolagus cuniculus). Int J Parasitol 35:1509–1515

  51. Lemaître J-F, Ramm SA, Barton RA, Stockley P (2009) Sperm competition and brain size evolution in mammals. J Evol Biol 22:2215–2221

  52. Lindenfors P, Nunn CL, Jones KE, Cunningham AA, Sechrest W, Gittleman JL (2007) Parasite species richness in carnivores: effects of host body mass, latitude, geographical range and population density. Glob Ecol Biogeogr 16:496–509

  53. Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87–98

  54. Luong LT, Grear DA, Hudson PJ (2009) Male hosts are responsible for the transmission of a trophically transmitted parasite, Pterygodermatites peromysci, to the intermediate host in the absence of sex-biased infection. Int J Parasitol 39:1263–1268

  55. Mace GM, Harvey PH, Clutton-Brock TH (1981) Brain size and ecology in small mammals. J Zool 193:333–354

  56. Maddison WP, Maddison DR (2009) Mesquite: a modular system for evolutionary analysis. Version 2.72. http://www.mesquiteproject.org

  57. Martins EP, Hansen TF (1997) Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. Am Nat 149:646–667

  58. Matthee S, McGeoch MA, Krasnov BR (2010) Parasite-specific variation and the extent of male-biased parasitism; an example with a South African rodent and ectoparasitic arthropods. Parasitology 137:651–660

  59. McNab BK, Eisenberg JF (1989) Brain size and its relation to the rate of metabolism in mammals. Am Nat 133:157–167

  60. Meier PT (1983) Relative brain size within the North American Sciuridae. J Mammal 64:642–647

  61. Midford PE, Garland T, Maddison WP (2008) PDAP:PDTREE package for Mesquite, version 1.14. http://www.mesquiteproject.org/pdap_mesquite/index.html

  62. Mills SC, Grapputo A, Jokinen I, Koskela E, Mappes T, Oksanen TA, Poikonen T (2009) Testosterone-mediated effects on fitness-related phenotypic traits and fitness. Am Nat 173:475–487

  63. Møller AP, Rozsa L (2005) Parasite biodiversity and host defences: chewing lice and immune response of their avian hosts. Oecologia 142:169–176

  64. Møller AP, Erritzoe J, Garamszegi Z (2005) Covariation between brain size and immunity in birds: implications for brain size evolution. J Evol Biol 18:223–237

  65. Morand S, Harvey PH (2000) Mammalian metabolism, longevity and parasite species richness. Proc R Soc Lond B 267:1999–2003

  66. Morand S, Poulin R (1998) Density, body mass and parasite species richness of terrestrial mammals. Evol Ecol 12:717–727

  67. Morand S, Poulin R (2000) Nematode parasite species richness and the evolution of spleen size in birds. Can J Zool 78:1356–1360

  68. Morand S, Gouy De Bellocq J, Stanko M, Miklisova D (2004) Is sex-biased ectoparasitism related to sexual size dimorphism in small mammals of Central Europe? Parasitology 129:505–510

  69. Moret Y, Schmid-Hempel P (2000) Survival for immunity: the price of immune system activation for bumblebee workers. Science 290:1166–1168

  70. Mougeot F, Redpath SM, Piertney SB, Hudson PJ (2005) Separating behavioral and physiological mechanisms in testosterone-mediated trade-offs. Am Nat 166:158–168

  71. Nikitina NA (1980) Mice. In: Sokolov VE (ed) Results of mammalian marking. Nauka, Moscow, pp 157–175 (in Russian)

  72. Nordling D, Andersson M, Zohari S, Gustafsson L (1998) Reproductive effort reduces specific immune response and parasite resistance. Proc R Soc Lond B 265:1291–1298

  73. Nunn CL, Barton RA (2000) Allometric slopes and independent contrasts: a comparative test of Kleiber’s law in primate ranging patterns. Am Nat 156:519–533

  74. Nunn CL, Altizer S, Jones KE, Sechrest W (2003) Comparative tests of parasites species richness in primates. Am Nat 162:597–614

  75. Nunn CL, Altizer S, Sechrest W, Jones KE, Barton RA, Gittleman JL (2004) Parasites and the evolutionary diversification of primates clades. Am Nat 164:90–103

  76. Pagel M (1997) Seeking the evolutionary regression coefficient: an analysis of what comparative methods measure. J Theor Biol 164:191–205

  77. Pagel M (1999) Inferring the biological patterns of evolution. Nature 401:877–884

  78. Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290

  79. Parapanov RN, Nusslé S, Crausaz M, Senn A, Hausser J, Vogel P (2009) Testis size, sperm characteristics and testosterone concentrations in four species of shrews (Mammalia, Soricidae). Anim Reprod Sci 114:269–278

  80. Parker GA, Ball MA, Stockley P, Gage MJG (1997) Sperm competition games: a prospective analysis of risk assessment. Proc R Soc Lond B 264:1793–1802

  81. Pitnick S, Jones KE, Wilkinson GS (2006) Mating system and brain size in bats. Proc R Soc Lond B 273:719–724

  82. Poulin R (1995) Phylogeny, ecology, and the richness of parasite communities in vertebrates. Ecol Monogr 65:283-302

  83. Poulin R, Morand S (2004) Parasite biodiversity. Smithsonian Institution Press, Washington

  84. Poulin R, Mouillot D (2004) The evolution of taxonomic diversity in helminth assemblages of mammalian hosts. Evol Ecol 18:231–247

  85. Radovsky FJ (1985) Evolution of mammalian mesostigmatid mites. In: Kim KS (ed) Coevolution of parasitic arthropods and mammals. Wiley, New York, pp 441–504

  86. Rolff J (2002) Bateman’s principle and immunity. Proc R Soc Lond B 269:867–872

  87. Safi K, Dechmann DKN (2005) Adaptation of brain regions to habitat complexity: a comparative analysis in bats (Chiroptera). Proc R Soc Lond B 272:179–186

  88. Schmid-Hempel P, Ebert D (2003) On the evolutionary ecology of specific immune defence. Trends Ecol Evol 18:27–32

  89. Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defenses and trade offs in evolutionary ecology. Trends Ecol Evol 11:317–321

  90. Silva M, Downing JA (1995) CRC handbook of mammalian body masses. CRC, Boca Raton

  91. Šimková A, Ottová E, Morand S (2006) MHC variability, life traits and parasite diversity of European cyprinid fish. Evol Ecol 20:465–467

  92. Šimková A, Lafond T, Ondrackova M, Jurajda P, Ottová E, Morand S (2008) Parasitism, life history traits and immune defence in cyprinid fish. BMC Evol Biol 8:29

  93. Smith KG, Hunt JL (2004) On the use of spleen mass as a measure of avian immune system strength. Oecologia 138:28–31

  94. Soulsbury CD (2010) Genetic patterns of paternity and testes size in mammals. PLoS ONE 5:e9581. doi:10.1371/journal.pone.0009581

  95. Tagiltsev AA (1957) On the relationships between parasitic and nidicolous Acari (in Russian). Med Parasitol Parasit Dis (Med Parazitol Parazit Bol) 26:440–447

  96. Taylor LH, Mackinnon MJ, Read AF (1998) Virulence of mixed-clone and single-clone infections of the rodent malaria Plasmodium chabaudi. Evolution 52:583–591

  97. R Development Core Team (2005) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org

  98. Vassallo AI, Echeverria AI (2009) Evolution of brain size in a highly diversifying lineage of subterranean rodent genus Ctenomys (Caviomorpha: Ctenomyidae). Brain Behav Evol 73:138–149

  99. Wakelin D (1996) Immunity to parasites: how parasitic infections are controlled, 2nd edn. Cambridge University Press, Cambridge

  100. Wedell N, Gage MJG, Parker GA (2002) Sperm competition, male prudence and sperm-limited females. Trends Ecol Evol 17:313–320

  101. Wegner KM, Reusch TBH, Kalbe M (2003) Multiple parasites are driving major histocompatibility complex polymorphism in the wild. J Evol Biol 16:224–232

  102. Zuk M, Mckean KA (1996) Sex differences in parasite infections: patterns and processes. Int J Parasitol 26:1009–1024

Download references

Acknowledgments

We thank Allan Degen for helpful comments on the earlier version of the manuscript. This study was partly supported by the Israel Science Foundation (grant no. 27/08 to B. R. K.). This is publication no. 686 of the Mitrani Department of Desert Ecology.

Author information

Correspondence to Boris R. Krasnov.

Additional information

Communicated by Klaus Fischer.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 195 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Bordes, F., Morand, S. & Krasnov, B.R. Does investment into “expensive” tissue compromise anti-parasitic defence? Testes size, brain size and parasite diversity in rodent hosts. Oecologia 165, 7–16 (2011). https://doi.org/10.1007/s00442-010-1743-9

Download citation

Keywords

  • Expensive tissue hypothesis
  • Brain
  • Parasites
  • Rodents
  • Species richness