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A dynamic threshold model for terminal investment

  • Kristin R. Duffield
  • E. Keith Bowers
  • Scott K. Sakaluk
  • Ben M. Sadd
Invited Review

Abstract

Although reproductive strategies can be influenced by a variety of intrinsic and extrinsic factors, life history theory provides a rigorous framework for explaining variation in reproductive effort. The terminal investment hypothesis proposes that a decreased expectation of future reproduction (as might arise from a mortality threat) should precipitate increased investment in current reproduction. Terminal investment has been widely studied, and a variety of intrinsic and extrinsic cues that elicit such a response have been identified across an array of taxa. Although terminal investment is often treated as a static strategy, the level at which a cue of decreased future reproduction is sufficient to trigger increased current reproductive effort (i.e., the terminal investment threshold) may depend on the context, including the internal state of the organism or its current external environment, independent of the cue that triggers a shift in reproductive investment. Here, we review empirical studies that address the terminal investment hypothesis, exploring both the intrinsic and extrinsic factors that mediate its expression. Based on these studies, we propose a novel framework within which to view the strategy of terminal investment, incorporating factors that influence an individual’s residual reproductive value beyond a terminal investment trigger—the dynamic terminal investment threshold.

Keywords

Residual reproductive value Life history evolution Condition-dependent reproductive investment Fecundity compensation Phenotypic plasticity 

Notes

Acknowledgements

We thank I. Krams and two anonymous reviewers for helpful comments that improved this manuscript.

Funding information

This research was funded, in part, by grants from the National Science Foundation IOS 16-54028 (SKS and BMS), Illinois State University Summer Faculty Fellowship and Faculty Research Award (SKS), and National Institutes of Health 2R15HD076308-02A1 (SKS and C.F. Thompson).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

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References

  1. Adamo SA (1999) Evidence for adaptive changes in egg laying in crickets exposed to bacteria and parasites. Anim Behav 57(1):117–124.  https://doi.org/10.1006/anbe.1998.0999 PubMedCrossRefGoogle Scholar
  2. Adamo SA, Jensen M, Younger M (2001) Changes in lifetime immunocompetence in male and female Gryllus texensis (formerly G. integer): trade-offs between immunity and reproduction. Anim Behav 62(3):417–425.  https://doi.org/10.1006/anbe.2001.1786 CrossRefGoogle Scholar
  3. Adamo SA, McKee R (2017) Differential effects of predator cues versus activation of fight-or-flight behaviour on reproduction in the cricket Gryllus texensis. Anim Behav 134:1–8.  https://doi.org/10.1016/j.anbehav.2017.09.027 CrossRefGoogle Scholar
  4. Ahmed AM, Baggott SL, Maingon R, Hurd H (2002) The costs of mounting an immune response are reflected in the reproductive fitness of the mosquito Anopheles gambiae. Oikos 97(3):371–377.  https://doi.org/10.1034/j.1600-0706.2002.970307.x CrossRefGoogle Scholar
  5. Ahtiainen JJ, Alatalo RV, Kortet R, Rantala MJ (2005) A trade-off between sexual signalling and immune function in a natural population of the drumming wolf spider Hygrolycosa rubrofasciata. J Evol Biol 18(4):985–991.  https://doi.org/10.1111/j.1420-9101.2005.00907.x PubMedCrossRefGoogle Scholar
  6. Alonso-Alvarez C, Bertrand S, Devevey G, Prost J, Faivre B, Sorci G (2004) Increased susceptibility to oxidative stress as a proximate cost of reproduction. Ecol Lett 7(5):363–368.  https://doi.org/10.1111/j.1461-0248.2004.00594.x CrossRefGoogle Scholar
  7. Altincicek B, Gross J, Vilcinskas A (2008) Wounding-mediated gene expression and accelerated viviparous reproduction of the pea aphid Acyrthosiphon pisum. Insect Mol Biol 17(6):711–716.  https://doi.org/10.1111/j.1365-2583.2008.00835.x PubMedCrossRefGoogle Scholar
  8. An D, Waldman B (2016) Enhanced call effort in Japanese tree frogs infected by amphibian chytrid fungus. Biol Lett 12(3):20160018.  https://doi.org/10.1098/rsbl.2016.0018 PubMedPubMedCentralCrossRefGoogle Scholar
  9. Baker JR (1938) The evolution of breeding seasons. In: de Beer GR (ed) Evolution: essays on aspects of evolutionary biology. Clarendon Press, Oxford, pp 161–177Google Scholar
  10. Barrett ELB, Hunt J, Moore AJ, Moore PJ (2009) Separate and combined effects of nutrition during juvenile and sexual development on female life-history trajectories: the thrifty phenotype in a cockroach. Proc R Soc B 276(1671):3257–3264.  https://doi.org/10.1098/rspb.2009.0725 PubMedCrossRefGoogle Scholar
  11. Barribeau SM, Sok D, Gerardo NM (2010) Aphid reproductive investment in response to mortality risks. BMC Evol Biol 10(1):251.  https://doi.org/10.1186/1471-2148-10-251 PubMedPubMedCentralCrossRefGoogle Scholar
  12. Benowitz KM, Head ML, Williams CA, Moore AJ, Royle NJ (2013) Male age mediates reproductive investment and response to paternity assurance. Proc R Soc B 280(1764):20131124.  https://doi.org/10.1098/rspb.2013.1124 PubMedCrossRefGoogle Scholar
  13. Bercovitch FB, Loomis CP, Rieches RG (2009) Age-specific changes in reproductive effort and terminal investment in female Nile lechwe. J Mammal 90(1):40–46.  https://doi.org/10.1644/08-MAMM-A-124.1 CrossRefGoogle Scholar
  14. Billing AM, Rosenqvist G, Berglund A (2007) No terminal investment in pipefish males: only young males exhibit risk-prone courtship behavior. Behav Ecol 18(3):535–540.  https://doi.org/10.1093/beheco/arm007 CrossRefGoogle Scholar
  15. Billman EJ, Belk MC (2014) Effect of age-based and environment-based cues on reproductive investment in Gambusia affinis. Ecol Evol 4(9):1611–1622.  https://doi.org/10.1002/ece3.1055 PubMedPubMedCentralCrossRefGoogle Scholar
  16. Blair L, Webster JP (2007) Dose-dependent schistosome-induced mortality and morbidity risk elevates host reproductive effort. J Evol Biol 20(1):54–61.  https://doi.org/10.1111/j.1420-9101.2006.01230.x PubMedCrossRefGoogle Scholar
  17. Bonds MH (2006) Host life-history strategy explains pathogen-induced sterility. Am Nat 168(3):281–293.  https://doi.org/10.1086/506922 PubMedCrossRefGoogle Scholar
  18. Bonneaud C, Mazuc J, Chastel O, Westerdahl H, Sorci G (2004) Terminal investment induced by immune challenge and fitness traits associated with major histocompatibility complex in the house sparrow. Evolution 58(12):2823–2830.  https://doi.org/10.1111/j.0014-3820.2004.tb01633.x PubMedCrossRefGoogle Scholar
  19. Boots M, Begon M (1993) Trade-offs with resistance to a granulosis virus in the Indian meal moth, examined by a laboratory evolution experiment. Funct Ecol 7(5):528–534.  https://doi.org/10.2307/2390128 CrossRefGoogle Scholar
  20. Bowers EK, Bowden RM, Sakaluk SK, Thompson CF (2015) Immune activation generates corticosterone-mediated terminal reproductive investment in a wild bird. Am Nat 185(6):769–783.  https://doi.org/10.1086/681017 PubMedPubMedCentralCrossRefGoogle Scholar
  21. Bowers EK, Smith RA, Hodges CJ, Zimmerman LM, Thompson CF, Sakaluk SK (2012) Sex-biased terminal investment in offspring induced by maternal immune challenge in the house wren (Troglodytes aedon). Proc R Soc B 279(1739):2891–2898.  https://doi.org/10.1098/rspb.2012.0443 PubMedCrossRefGoogle Scholar
  22. Brannelly LA, Webb R, Skerratt LF, Berger L (2016) Amphibians with infectious disease increase their reproductive effort: evidence for the terminal investment hypothesis. Open Biol 6(6):150251.  https://doi.org/10.1098/rsob.150251 PubMedPubMedCentralCrossRefGoogle Scholar
  23. Brey PT, Lee WJ, Yamakawa M, Koizumi Y, Perrot S, François M, Ashida M (1993) Role of the integument in insect immunity: epicuticular abrasion and induction of cecropin synthesis in cuticular epithelial cells. P Natl Acad Sci USA 90(13):6275–6279.  https://doi.org/10.1073/pnas.90.13.6275 CrossRefGoogle Scholar
  24. Brown GP, Shine R (2002) Reproductive ecology of a tropical natricine snake, Tropidonophis mairii (Colubridae). J Zool 258(1):63–72.  https://doi.org/10.1017/S0952836902001218 CrossRefGoogle Scholar
  25. Brown WD (1997) Female remating and the intensity of female choice in black-horned tree crickets, Oecanthus nigricornis. Behav Ecol 8(1):66–74.  https://doi.org/10.1093/beheco/8.1.66 CrossRefGoogle Scholar
  26. Buckling A, Ranford-Cartwright LC, Miles A, Read AF (1999) Chloroquine increases Plasmodium falciparum gametocytogenesis in vitro. Parasitology 118(4):339–346.  https://doi.org/10.1017/S0031182099003960 PubMedCrossRefGoogle Scholar
  27. Buckling AG, Taylor LH, Carlton JM, Read AF (1997) Adaptive changes in Plasmodium transmission strategies following chloroquine chemotherapy. Proc R Soc Lond B 264:552–559CrossRefGoogle Scholar
  28. Calow P (1979) The cost of reproduction—a physiological approach. Biol Rev 54(1):23–40.  https://doi.org/10.1111/j.1469-185X.1979.tb00866.x PubMedCrossRefGoogle Scholar
  29. Carter LM, Kafsack BF, Llinás M, Mideo N, Pollitt LC, Reece SE (2013) Stress and sex in malaria parasites: why does commitment vary? Evol Med Public Health 2013(1):135–147.  https://doi.org/10.1093/emph/eot011 PubMedPubMedCentralCrossRefGoogle Scholar
  30. Chadwick W, Little TJ (2005) A parasite-mediated life-history shift in Daphnia magna. Proc R Soc B 272(1562):505–509.  https://doi.org/10.1098/rspb.2004.2959 PubMedCrossRefGoogle Scholar
  31. Clutton-Brock TH (1984) Reproductive effort and terminal investment in iteroparous animals. Am Nat 123(2):212–229.  https://doi.org/10.1086/284198 CrossRefGoogle Scholar
  32. Clutton-Brock TH, Guinness FE, Albon SD (1982) Red deer: behavior and ecology of two sexes. University of Chicago Press, ChicagoGoogle Scholar
  33. Cockrem JF (1995) Timing of seasonal breeding in birds, with particular reference to New Zealand birds. Reprod Fert Develop 7(1):1–19.  https://doi.org/10.1071/RD9950001 CrossRefGoogle Scholar
  34. Coltman DW, Festa-Bianchet M, Jorgenson JT, Strobeck C (2002) Age-dependent sexual selection in bighorn rams. Proc R Soc Lond B 269(1487):165–172.  https://doi.org/10.1098/rspb.2001.1851 CrossRefGoogle Scholar
  35. Copeland EK, Fedorka KM (2012) The influence of male age and simulated pathogenic infection on producing a dishonest sexual signal. Proc R Soc B 279(1748):4740–4746.  https://doi.org/10.1098/rspb.2012.1914 PubMedCrossRefGoogle Scholar
  36. Côté SD, Festa-Bianchet M (2001) Reproductive success in female mountain goats: the influence of age and social rank. Anim Behav 62(1):173–181.  https://doi.org/10.1006/anbe.2001.1719 CrossRefGoogle Scholar
  37. Cotter SC, Kruuk LEB, Wilson K (2004) Costs of resistance: genetic correlations and potential trade-offs in an insect immune system. J Evol Biol 17(2):421–429PubMedCrossRefGoogle Scholar
  38. Cotter SC, Simpson SJ, Raubenheimer D, Wilson K (2011) Macronutrient balance mediates trade-offs between immune function and life history traits. Funct Ecol 25(1):186–198.  https://doi.org/10.1111/j.1365-2435.2010.01766.x CrossRefGoogle Scholar
  39. Cotter SC, Ward RJS, Kilner RM (2010) Age-specific reproductive investment in female burying beetles: independent effects of state and risk of death. Funct Ecol 25:652–660CrossRefGoogle Scholar
  40. Creighton JC, Heflin ND, Belk MC (2009) Cost of reproduction, resource quality, and terminal investment in a burying beetle. Am Nat 174(5):673–684.  https://doi.org/10.1086/605963 PubMedCrossRefGoogle Scholar
  41. Curio E (1983) Why do young birds reproduce less well? Ibis 125:400–404CrossRefGoogle Scholar
  42. Derting TL, Virk MK (2005) Positive effects of testosterone and immunochallenge on energy allocation to reproductive organs. J Comp Physiol B 175(8):543–556.  https://doi.org/10.1007/s00360-005-0015-1 PubMedCrossRefGoogle Scholar
  43. Descamps S, Boutin S, Berteaux D, Gaillard J-M (2007) Female red squirrels fit Williams’ hypothesis of increasing reproductive effort with increasing age. J Anim Ecol 76(6):1192–1201.  https://doi.org/10.1111/j.1365-2656.2007.01301.x PubMedCrossRefGoogle Scholar
  44. Drent RH, Daan S (1980) The prudent parent: energetic adjustments in avian breeding. Ardea 38–90:225–252Google Scholar
  45. Duffield KR, Hunt J, Rapkin J, Sadd BM, Sakaluk SK (2015) Terminal investment in the gustatory appeal of nuptial food gifts in crickets. J Evol Biol 28(10):1872–1881.  https://doi.org/10.1111/jeb.12703 PubMedCrossRefGoogle Scholar
  46. Durso AM, French SS (2017) Stable isotope tracers reveal a trade-off between reproduction and immunity in a reptile with competing needs. Funct Ecol (published online),  https://doi.org/10.1111/1365-2435.13002)
  47. Ericsson G, Wallin K, Ball JP, Broberg M (2001) Age-related reproductive effort and senescence in free-ranging moose, Alces alces. Ecology 82(6):1613–1620.  https://doi.org/10.1890/0012-9658(2001)082[1613:ARREAS]2.0.CO;2 CrossRefGoogle Scholar
  48. Fedorka KM, Mousseau TA (2002) Material and genetic benefits of female multiple mating and polyandry. Anim Behav 64(3):361–367.  https://doi.org/10.1006/anbe.2002.3052 CrossRefGoogle Scholar
  49. Fessler DMT, Navarrete CD, Hopkins W, Izard MK (2005) Examining the terminal investment hypothesis in humans and chimpanzees: associations among maternal age, parity, and birth weight. Am J Phys Anthropol 127(1):95–104.  https://doi.org/10.1002/ajpa.20039 PubMedCrossRefGoogle Scholar
  50. Festa-Bianchet M (1988) Nursing behaviour of bighorn sheep: correlates of ewe age, parasitism, lamb age, birthdate and sex. Anim Behav 36(5):1445–1454.  https://doi.org/10.1016/S0003-3472(88)80215-X CrossRefGoogle Scholar
  51. Fisher RA (1930) The genetical theory of natural selection. Clarendon Press, Oxford.  https://doi.org/10.5962/bhl.title.27468 CrossRefGoogle Scholar
  52. Forslund P, Pärt T (1995) Age and reproduction in birds—hypotheses and tests. Trends Ecol Evol 10(9):374–378.  https://doi.org/10.1016/S0169-5347(00)89141-7 PubMedCrossRefGoogle Scholar
  53. Fricke C, Bretman A, Chapman T (2008) Adult male nutrition and reproductive success in Drosophila melanogaster. Evolution 62(12):3170–3177.  https://doi.org/10.1111/j.1558-5646.2008.00515.x PubMedCrossRefGoogle Scholar
  54. Gadgil M, Bossert WH (1970) Life historical consequences of natural selection. Am Nat 104(935):1–24.  https://doi.org/10.1086/282637 CrossRefGoogle Scholar
  55. Gandon S, Agnew P, Michalakis Y (2002) Coevolution between parasite virulence and host life-history traits. Am Nat 160(3):374–388.  https://doi.org/10.1086/341525 PubMedCrossRefGoogle Scholar
  56. Giehr J, Grasse AV, Cremer S, Heinze J, Schrempf A (2017) Ant queens increase their reproductive efforts after pathogen infection. R Soc Open Sci 4(7):170547.  https://doi.org/10.1098/rsos.170547 PubMedPubMedCentralCrossRefGoogle Scholar
  57. González-Tokman DM, González-Santoyo I, Córdoba-Aguilar A (2013) Mating success and energetic condition effects driven by terminal investment in territorial males of a short-lived invertebrate. Funct Ecol 27(3):739–747.  https://doi.org/10.1111/1365-2435.12072 CrossRefGoogle Scholar
  58. Graham AL, Hayward AD, Watt KA, Pilkington JG, Pemberton JM, Nussey DH (2010) Fitness correlates of heritable variation in antibody responsiveness in a wild mammal. Science 330(6004):662–665.  https://doi.org/10.1126/science.1194878 PubMedCrossRefGoogle Scholar
  59. Guivier E, Lippens C, Faivre B, Sorci G (2017) Plastic and micro-evolutionary responses of a nematode to the host immune environment. Exp Parasitol 181:14–22.  https://doi.org/10.1016/j.exppara.2017.07.002 PubMedCrossRefGoogle Scholar
  60. Gustafsson L, Nordling D, Andersson MS, Sheldon BC, Qvarnstrom A (1994) Infectious diseases, reproductive effort and the cost of reproduction in birds. Philos T Roy Soc B 346(1317):323–331.  https://doi.org/10.1098/rstb.1994.0149 CrossRefGoogle Scholar
  61. Hamilton WD (1980) Sex versus non-sex versus parasite. Oikos 35(2):282–290.  https://doi.org/10.2307/3544435 CrossRefGoogle Scholar
  62. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218(4570):384–387.  https://doi.org/10.1126/science.7123238 PubMedCrossRefGoogle Scholar
  63. Hanssen SA (2006) Costs of an immune challenge and terminal investment in a long-lived bird. Ecology 87(10):2440–2446.  https://doi.org/10.1890/0012-9658(2006)87[2440:COAICA]2.0.CO;2 PubMedCrossRefGoogle Scholar
  64. Harshman LG, Zera AJ (2007) The cost of reproduction: the devil in the details. Trends Ecol Evol 22(2):80–86.  https://doi.org/10.1016/j.tree.2006.10.008 PubMedCrossRefGoogle Scholar
  65. Heino M, Kaitala V (1999) Evolution of resource allocation between growth and reproduction in animals with indeterminate growth. J Evol Biol 12(3):423–429.  https://doi.org/10.1046/j.1420-9101.1999.00044.x CrossRefGoogle Scholar
  66. Heinze J, Schrempf A (2012) Terminal investment: individual reproduction of ant queens increases with age. PLoS One 7(4):e35201.  https://doi.org/10.1371/journal.pone.0035201 PubMedPubMedCentralCrossRefGoogle Scholar
  67. Hendry TA, Clark KJ, Baltrus DA (2016) A highly infective plant-associated bacterium influences reproductive rates in pea aphids. R Soc Open Sci 3(2):150478.  https://doi.org/10.1098/rsos.150478 PubMedPubMedCentralCrossRefGoogle Scholar
  68. Hill K, Kaplan H (1999) Life history traits in humans: theory and empirical studies. Annu Rev Anthropol 28(1):397–430.  https://doi.org/10.1146/annurev.anthro.28.1.397 PubMedCrossRefGoogle Scholar
  69. Hirshfield MF, Tinkle DW (1975) Natural selection and the evolution of reproductive effort. P Natl Acad Sci USA 72(6):2227–2231.  https://doi.org/10.1073/pnas.72.6.2227 CrossRefGoogle Scholar
  70. Hoffman CL, Higham JP, Mas-Rivera A, Ayala JE, Maestripieri D (2010) Terminal investment and senescence in rhesus macaques (Macaca mulatta) on Cayo Santiago. Behav Ecol 21(5):972–978.  https://doi.org/10.1093/beheco/arq098 PubMedPubMedCentralCrossRefGoogle Scholar
  71. Hunt J, Brooks R, Jennions MD, Smith MJ, Bentsen CL, Bussière LF (2004) High-quality male field crickets invest heavily in sexual display but die young. Nature 432(7020):1024–1027.  https://doi.org/10.1038/nature03084 PubMedCrossRefGoogle Scholar
  72. Hurd H (2001) Host fecundity reduction: a strategy for damage limitation? Trends Parasitol 17(8):363–368.  https://doi.org/10.1016/S1471-4922(01)01927-4 PubMedCrossRefGoogle Scholar
  73. Ilmonen P, Taarna T, Hasselquist D (2000) Experimentally activated immune defence in female pied flycatchers results in reduced breeding success. Proc R Soc Lond B 267(1444):665–670.  https://doi.org/10.1098/rspb.2000.1053 CrossRefGoogle Scholar
  74. Ivy TM, Sakaluk SK (2005) Polyandry promotes enhanced offspring survival in decorated crickets. Evolution 59(1):152–159.  https://doi.org/10.1111/j.0014-3820.2005.tb00902.x PubMedCrossRefGoogle Scholar
  75. Jacot A, Scheuber H, Brinkhof MWG, Shaw K (2004) Costs of an induced immune response on sexual display and longevity in field crickets. Evolution 58(10):2280–2286.  https://doi.org/10.1111/j.0014-3820.2004.tb01603.x PubMedCrossRefGoogle Scholar
  76. Javoiš J (2013) A two-resource model of terminal investment. Theory Biosci 132(2):123–132.  https://doi.org/10.1007/s12064-013-0176-5 PubMedCrossRefGoogle Scholar
  77. Jennings DJ, Carlin CM, Hayden TJ, Gammell MP (2010) Investment in fighting in relation to body condition, age and dominance rank in the male fallow deer, Dama dama. Anim Behav 79(6):1293–1300.  https://doi.org/10.1016/j.anbehav.2010.02.031 CrossRefGoogle Scholar
  78. Jönsson KI (1997) Capital and income breeding as alternative tactics of resource use in reproduction. Oikos 78(1):57–66.  https://doi.org/10.2307/3545800 CrossRefGoogle Scholar
  79. Judge KA, De Luca PA, Morris GK (2011) Food limitation causes female haglids to mate more often. Can J Zool 89(10):992–998.  https://doi.org/10.1139/z11-078 CrossRefGoogle Scholar
  80. Karell P, Pietiäinen H, Siitari H, Brommer JE (2007) A possible link between parasite defence and residual reproduction. J Evol Biol 20(6):2248–2252.  https://doi.org/10.1111/j.1420-9101.2007.01423.x PubMedCrossRefGoogle Scholar
  81. Kight SL, Batino M, Zhang Z (2000) Temperature-dependent parental investment in the giant waterbug Belostoma flumineum (Heteroptera: Belostomatidae). Ann Entomol Soc Am 93(2):340–342.  https://doi.org/10.1603/0013-8746(2000)093[0340:TDPIIT]2.0.CO;2 CrossRefGoogle Scholar
  82. Kivleniece I, Krams I, Daukšte J, Krama T, Rantala MJ (2010) Sexual attractiveness of immune-challenged male mealworm beetles suggests terminal investment in reproduction. Anim Behav 80(6):1015–1021.  https://doi.org/10.1016/j.anbehav.2010.09.004 CrossRefGoogle Scholar
  83. Koenig WD, Knops JMH, Carmen WJ, Pesendorfer MB (2017) Testing the terminal investment hypothesis in California oaks. Am Nat 189(5):564–569.  https://doi.org/10.1086/691161 PubMedCrossRefGoogle Scholar
  84. Kolluru GR, Grether GF (2005) The effects of resource availability on alternative mating tactics in guppies (Poecilia reticulata). Behav Ecol 16(1):294–300.  https://doi.org/10.1093/beheco/arh161 CrossRefGoogle Scholar
  85. Korpimäki E, Norrdahl K, Valkama J (1994) Reproductive investment under fluctuating predation risk: microtine rodents and small mustelids. Evol Ecol 8(4):357–368.  https://doi.org/10.1007/BF01238188 CrossRefGoogle Scholar
  86. Krams I, Daukšte J, Kivleniece I, Krama T, Rantala MJ, Ramey G, Šauša L (2011) Female choice reveals terminal investment in male mealworm beetles, Tenebrio molitor, after a repeated activation of the immune system. J Insect Sci 11(56):1–14.  https://doi.org/10.1673/031.011.5601 CrossRefGoogle Scholar
  87. Krams IA, Krama T, Moore FR, Rantala MJ, Mänd R, Mierauskas P, Mänd M (2015) Resource availability as a proxy for terminal investment in a beetle. Oecologia 178(2):339–345.  https://doi.org/10.1007/s00442-014-3210-5 PubMedCrossRefGoogle Scholar
  88. Kubička L, Kratochvíl L (2009) First grow, then breed and finally get fat: herarchical allocation to life-history traits in a lizard with invariant clutch size. Funct Ecol 23(3):595–601.  https://doi.org/10.1111/j.1365-2435.2008.01518.x CrossRefGoogle Scholar
  89. Lafaille M, Bimbard G, Greenfield MD (2010) Risk trading in mating behavior: forgoing anti-predator responses reduces the likelihood of missing terminal mating opportunities. Behav Ecol Sociobiol 64(9):1485–1494.  https://doi.org/10.1007/s00265-010-0963-7 CrossRefGoogle Scholar
  90. Langley PA, Clutton-Brock TH (1998) Does reproductive investment change with age in tsetse flies, Glossina morsitans morsitans (Diptera: Glossinidae)? Funct Ecol 12(6):866–870.  https://doi.org/10.1046/j.1365-2435.1998.00262.x CrossRefGoogle Scholar
  91. Lardner B, Loman J (2003) Growth or reproduction? Resource allocation by female frogs Rana temporaria. Oecologia 137(4):541–546.  https://doi.org/10.1007/s00442-003-1390-5 PubMedCrossRefGoogle Scholar
  92. Lawniczak MKN, Barnes AI, Linklater JR, Boone JM, Wigby S, Chapman T (2007) Mating and immunity in invertebrates. Trends Ecol Evol 22(1):48–55.  https://doi.org/10.1016/j.tree.2006.09.012 PubMedCrossRefGoogle Scholar
  93. Leman JC, Weddle CB, Gershman SN, Kerr AM, Ower GD, St John JM, Vogel LA, Sakaluk SK (2009) Lovesick: immunological costs of mating to male sagebrush crickets. J Evol Biol 22(1):163–171.  https://doi.org/10.1111/j.1420-9101.2008.01636.x PubMedCrossRefGoogle Scholar
  94. Leonardo TE, Mondor EB (2006) Symbiont modifies host life-history traits that affect gene flow. Proc R Soc B 273(1590):1079–1084.  https://doi.org/10.1098/rspb.2005.3408 PubMedCrossRefGoogle Scholar
  95. Leventhal GE, Dünner RP, Barribeau SM (2014) Delayed virulence and limited costs promote fecundity compensation upon infection. Am Nat 183(4):480–493.  https://doi.org/10.1086/675242 PubMedCrossRefGoogle Scholar
  96. Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88(1):87–98.  https://doi.org/10.1034/j.1600-0706.2000.880110.x CrossRefGoogle Scholar
  97. Loison A, Festa-Bianchet M, Gaillard J-M, Jorgenson JT, Jullien J-M (1999) Age-specific survival in five populations of ungulates: evidence of senescence. Ecology 80(8):2539–2554.  https://doi.org/10.1890/0012-9658(1999)080[2539:ASSIFP]2.0.CO;2 CrossRefGoogle Scholar
  98. Lopes PC, Adelman J, Wingfield JC, Bentley GE (2012) Social context modulates sickness behavior. Behav Ecol Sociobiol 66(10):1421–1428.  https://doi.org/10.1007/s00265-012-1397-1 CrossRefGoogle Scholar
  99. Luong LT, Polak M (2007) Costs of resistance in the DrosophilaMacrocheles system: a negative genetic correlation between ectoparasite resistance and reproduction. Evolution 61(6):1391–1402.  https://doi.org/10.1111/j.1558-5646.2007.00116.x PubMedCrossRefGoogle Scholar
  100. Luu H, Tate AT (2017) Recovery and immune priming modulate the evolutionary trajectory of infection-induced reproductive strategies. J Evol Biol (published online).  https://doi.org/10.1111/jeb.13138)  https://doi.org/10.1111/jeb.13138)
  101. Maher CR, Byers JA (1987) Age-related changes in reproductive effort of male bison. Behav Ecol Sociobiol 21(2):91–96.  https://doi.org/10.1007/BF02395436 CrossRefGoogle Scholar
  102. Marzal A, Bensch S, Reviriego M, Balbontin J, de Lope F (2008) Effects of malaria double infection in birds: one plus one is not two. J Evol Biol 21(4):979–987.  https://doi.org/10.1111/j.1420-9101.2008.01545.x PubMedCrossRefGoogle Scholar
  103. Mauck RA, Huntington CE, Grubb TC, Benkman C (2004) Age-specific reproductive success: evidence for the selection hypothesis. Evolution 58(4):880–885.  https://doi.org/10.1111/j.0014-3820.2004.tb00419.x PubMedCrossRefGoogle Scholar
  104. Minchella DJ (1985) Host life-history variation in response to parasitism. Parasitology 90(01):205–216.  https://doi.org/10.1017/S0031182000049143 CrossRefGoogle Scholar
  105. Minchella DJ, Loverde PT (1981) A cost of increased early reproductive effort in the snail Biomphalaria glabrata. Am Nat 118(6):876–881.  https://doi.org/10.1086/283879 CrossRefGoogle Scholar
  106. Morrow EH, Arnqvist G, Pitnick S (2003) Adaptation versus pleiotropy: why do males harm their mates? Behav Ecol 14(6):802–806.  https://doi.org/10.1093/beheco/arg073 CrossRefGoogle Scholar
  107. Nielsen ML, Holman L (2012) Terminal investment in multiple sexual signals: immune-challenged males produce more attractive pheromones. Funct Ecol 26(1):20–28.  https://doi.org/10.1111/j.1365-2435.2011.01914.x CrossRefGoogle Scholar
  108. Noonburg EG, Nisbet RM, McCauley E, Gurney WSC, Murdoch WW, de Roos AM (1998) Experimental testing of dynamic energy budget models. Funct Ecol 12(2):211–222.  https://doi.org/10.1046/j.1365-2435.1998.00174.x CrossRefGoogle Scholar
  109. Norris K, Anwar M, Read AF (1994) Reproductive effort influences the prevalence of haematozoan parasites in great tits. J Anim Ecol 63(3):601–610.  https://doi.org/10.2307/5226 CrossRefGoogle Scholar
  110. Ohlsson T, Smith HG, Råberg L, Hasselquist D (2002) Pheasant sexual ornaments reflect nutritional conditions during early growth. Proc R Soc Lond B 269(1486):21–27.  https://doi.org/10.1098/rspb.2001.1848 CrossRefGoogle Scholar
  111. Paitz RT, Harms HK, Bowden RM, Janzen FJ (2007) Experience pays: offspring survival increases with female age. Biol Lett 3(1):44–46.  https://doi.org/10.1098/rsbl.2006.0573 PubMedCrossRefGoogle Scholar
  112. Parker BJ, Barribeau SM, Laughton AM, de Roode JC, Gerardo NM (2011) Non-immunological defense in an evolutionary framework. Trends Ecol Evol 26(5):242–248.  https://doi.org/10.1016/j.tree.2011.02.005 PubMedCrossRefGoogle Scholar
  113. Part T, Gustafsson L, Moreno J (1992) “Terminal investment” and a sexual conflict in the collared flycatcher (Ficedula albicollis). Am Nat 140(5):868–882.  https://doi.org/10.1086/285445 PubMedCrossRefGoogle Scholar
  114. Perrin N, Sibly RM (1993) Dynamic models of energy allocation and investment. Annu Rev Ecol Syst 24(1):379–410.  https://doi.org/10.1146/annurev.es.24.110193.002115 CrossRefGoogle Scholar
  115. Pianka ER, Parker WS (1975) Age-specific reproductive tactics. Am Nat 109(968):453–464.  https://doi.org/10.1086/283013 CrossRefGoogle Scholar
  116. Podmokła E, Dubiec A, Drobniak SM, Arct A, Gustafsson CM (2014) Avian malaria is associated with increased reproductive investment in the blue tit. J Avian Biol 45(3):219–224.  https://doi.org/10.1111/j.1600-048X.2013.00284.x CrossRefGoogle Scholar
  117. Poisot T, Bell T, Martinez E, Gougat-Barbera C, Hochberg ME (2013) Terminal investment induced by a bacteriophage in a rhizosphere bacterium. F1000Research1:21Google Scholar
  118. Polak M, Starmer WT (1998) Parasite-induced risk of mortality elevates reproductive effort in male Drosophila. Proc R Soc Lond B 265(1411):2197–2201.  https://doi.org/10.1098/rspb.1998.0559 CrossRefGoogle Scholar
  119. Poveda K, Steffan-Dewenter I, Scheu S, Tscharntke T (2003) Effects of below- and above-ground herbivores on plant growth, flower visitation and seed set. Oecologia 135(4):601–605.  https://doi.org/10.1007/s00442-003-1228-1 PubMedCrossRefGoogle Scholar
  120. Pugesek BH (1981) Increased reproductive effort with age in the California gull (Larus californicus). Science 212(4496):822–823.  https://doi.org/10.1126/science.212.4496.822 PubMedCrossRefGoogle Scholar
  121. Pugesek BH (1983) The relationship between parental age and reproductive effort in the California gull (Larus californicus). Behav Ecol Sociobiol 13(3):161–171.  https://doi.org/10.1007/BF00299919 CrossRefGoogle Scholar
  122. Reaney LT, Knell RJ (2010) Immune activation but not male quality affects female current reproductive investment in a dung beetle. Behav Ecol 21(6):1367–1372.  https://doi.org/10.1093/beheco/arq139 CrossRefGoogle Scholar
  123. Rebar D, Greenfield MD (2017) When do acoustic cues matter? Perceived competition and reproductive plasticity over lifespan in a bushcricket. Anim Behav 128:41–49.  https://doi.org/10.1016/j.anbehav.2017.03.003 CrossRefGoogle Scholar
  124. Reznick D (1985) Costs of reproduction: an evaluation of the empirical evidence. Oikos 44(2):257–267.  https://doi.org/10.2307/3544698 CrossRefGoogle Scholar
  125. Roff DA (1992) The evolution of life histories: theory and analysis. Chapman and Hall, LondonGoogle Scholar
  126. Roff DA (2002) Life history evolution. Sinauer, Sunderland, MAGoogle Scholar
  127. Roff DA, Fairbairn DJ (2007) The evolution of trade-offs: where are we? J Evol Biol 20(2):433–447.  https://doi.org/10.1111/j.1420-9101.2006.01255.x PubMedCrossRefGoogle Scholar
  128. Roznik EA, Sapsford SJ, Pike DA, Schwarzkopf L, Alford RA (2015) Condition-dependent reproductive effort in frogs infected by a widespread pathogen. Proc R Soc B 282(1810):20150694.  https://doi.org/10.1098/rspb.2015.0694 PubMedCrossRefGoogle Scholar
  129. Sadd B, Holman L, Armitage H, Lock F, Marland R, Siva-Jothy MT (2006) Modulation of sexual signalling by immune challenged male mealworm beetles (Tenebrio molitor, L.): evidence for terminal investment and dishonesty. J Evol Biol 19(2):321–325.  https://doi.org/10.1111/j.1420-9101.2005.01062.x PubMedCrossRefGoogle Scholar
  130. Sadd BM, Schmid-Hempel P (2009) Principles of ecological immunology. Evol Appl 2(1):113–121.  https://doi.org/10.1111/j.1752-4571.2008.00057.x PubMedCrossRefGoogle Scholar
  131. Sanz JJ, Arriero E, Moreno J, Merino S (2001) Interactions between hemoparasite status and female age in the primary reproductive output of pied flycatchers. Oecologia 126(3):339–344.  https://doi.org/10.1007/s004420000530 PubMedCrossRefGoogle Scholar
  132. Schluter D, Price TD, Rowe L (1991) Conflicting selection pressures and life history trade-offs. Proc R Soc Lond B 246(1315):11–17.  https://doi.org/10.1098/rspb.1991.0118 CrossRefGoogle Scholar
  133. Schwanz LE (2008a) Persistent effects of maternal parasitic infection on offspring fitness: implications for adaptive reproductive strategies when parasitized. Funct Ecol 22(4):691–698.  https://doi.org/10.1111/j.1365-2435.2008.01397.x CrossRefGoogle Scholar
  134. Schwanz LE (2008b) Chronic parasitic infection alters reproductive output in deer mice. Behav Ecol Sociobiol 62(8):1351–1358.  https://doi.org/10.1007/s00265-008-0563-y CrossRefGoogle Scholar
  135. Schwenke RA, Lazzaro BP, Wolfner MF (2016) Reproduction–immunity trade-offs in insects. Annu Rev Entomol 61(1):239–256.  https://doi.org/10.1146/annurev-ento-010715-023924 PubMedCrossRefGoogle Scholar
  136. Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11(8):317–321.  https://doi.org/10.1016/0169-5347(96)10039-2 PubMedCrossRefGoogle Scholar
  137. Shoemaker KL, Adamo SA (2007) Adult female crickets, Gryllus texensis, maintain reproductive output after repeated immune challenges. Physiol Entomol 32(2):113–120.  https://doi.org/10.1111/j.1365-3032.2006.00552.x CrossRefGoogle Scholar
  138. Shoemaker KL, Parsons NM, Adamo SA (2006) Egg-laying behaviour following infection in the cricket Gryllus texensis. Can J Zool 84(3):412–418.  https://doi.org/10.1139/z06-013 CrossRefGoogle Scholar
  139. Simmons LW, Gwynne DT (1991) The refractory period of female katydids (Orthoptera: Tettigoniidae): sexual conflict over the remating interval? Behav Ecol 2(4):276–282.  https://doi.org/10.1093/beheco/2.4.276 CrossRefGoogle Scholar
  140. Simmons LW, Roberts B (2005) Bacterial immunity traded for sperm viability in male crickets. Science 309(5743):2031.  https://doi.org/10.1126/science.1114500 PubMedCrossRefGoogle Scholar
  141. Stahlschmidt ZR, Rollinson N, Acker M, Adamo SA (2013) Are all eggs created equal? Food availability and the fitness trade-off between reproduction and immunity. Funct Ecol 27(3):800–806.  https://doi.org/10.1111/1365-2435.12071 CrossRefGoogle Scholar
  142. Staudacher H, Menken SBJ, Groot AT (2015) Effects of immune challenge on the oviposition strategy of a noctuid moth. J Evol Biol 28(8):1568–1577.  https://doi.org/10.1111/jeb.12677 PubMedCrossRefGoogle Scholar
  143. Stearns SC (1989) Trade-offs in life-history evolution. Funct Ecol 3(3):259–268.  https://doi.org/10.2307/2389364 CrossRefGoogle Scholar
  144. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  145. Svensson E, RÅberg L, Koch C, Hasselquist D (1998) Energetic stress, immunosuppression and the costs of an antibody response. Funct Ecol 12(6):912–919.  https://doi.org/10.1046/j.1365-2435.1998.00271.x CrossRefGoogle Scholar
  146. Tarwater CE, Arcese P (2017) Age and years to death disparately influence reproductive allocation in a short-lived bird. Ecology 98(9):2248–2254.  https://doi.org/10.1002/ecy.1851 PubMedCrossRefGoogle Scholar
  147. Thanda Win A, Kojima W, Ishikawa Y (2013) Age-related male reproductive investment in courtship display and nuptial gifts in a moth, Ostrinia scapulalis. Ethology 119(4):325–334.  https://doi.org/10.1111/eth.12069 CrossRefGoogle Scholar
  148. Thomas SC (2011) Age-related changes in tree growth and functional biology: the role of reproduction. In: Meinzer FC, Lachenbruch B, Dawson TE (eds) Size- and age-related changes in tree structure and function. Springer, Dordrecht, NL, pp 33–64Google Scholar
  149. Uller T, Isaksson C, Olsson M (2006) Immune challenge reduces reproductive output and growth in a lizard. Funct Ecol 20(5):873–879.  https://doi.org/10.1111/j.1365-2435.2006.01163.x CrossRefGoogle Scholar
  150. Vale PF, Little TJ (2012) Fecundity compensation and tolerance to a sterilizing pathogen in Daphnia. J Evol Biol 25(9):1888–1896.  https://doi.org/10.1111/j.1420-9101.2012.02579.x PubMedPubMedCentralCrossRefGoogle Scholar
  151. van Noordwijk AJ, de Jong G (1986) Acquisition and allocation of resources: their influence on variation in life history tactics. Am Nat 128(1):137–142.  https://doi.org/10.1086/284547 CrossRefGoogle Scholar
  152. Varpe Ø, Jørgensen C, Tarling GA, Fiksen Ø (2009) The adaptive value of energy storage and capital breeding in seasonal environments. Oikos 118(3):363–370.  https://doi.org/10.1111/j.1600-0706.2008.17036.x CrossRefGoogle Scholar
  153. Velando A, Drummond H, Torres R (2006) Senescent birds redouble reproductive effort when ill: confirmation of the terminal investment hypothesis. Proc R Soc B 273(1593):1443–1448.  https://doi.org/10.1098/rspb.2006.3480 PubMedCrossRefGoogle Scholar
  154. Wagner WE Jr, Hoback WW (1999) Nutritional effects on male calling behaviour in the variable field cricket. Anim Behav 57(1):89–95.  https://doi.org/10.1006/anbe.1998.0964 PubMedCrossRefGoogle Scholar
  155. Warner DA, Lovern MB, Shine R (2007) Maternal nutrition affects reproductive output and sex allocation in a lizard with environmental sex determination. Proc R Soc B 274(1611):883–890.  https://doi.org/10.1098/rspb.2006.0105 PubMedCrossRefGoogle Scholar
  156. Weil ZM, Martin LB, Workman JL, Nelson RJ (2006) Immune challenge retards seasonal reproductive regression in rodents: evidence for terminal investment. Biol Lett 2(3):393–396.  https://doi.org/10.1098/rsbl.2006.0475 PubMedPubMedCentralCrossRefGoogle Scholar
  157. Weladji RB, Mysterud A, Holand Ø, Lenvik D (2002) Age-related reproductive effort in reindeer (Rangifer tarandus): evidence of senescence. Oecologia 131(1):79–82.  https://doi.org/10.1007/s00442-001-0864-6 PubMedCrossRefGoogle Scholar
  158. Wigby S, Domanitskaya EV, Choffat Y, Kubli E, Chapman T (2008) The effect of mating on immunity can be masked by experimental piercing in female Drosophila melanogaster. J Insect Physiol 54(2):414–420.  https://doi.org/10.1016/j.jinsphys.2007.10.010 PubMedCrossRefGoogle Scholar
  159. Williams GC (1966) Natural selection, the costs of reproduction, and a refinement of Lack’s principle. Am Nat 100(916):687–690.  https://doi.org/10.1086/282461 CrossRefGoogle Scholar
  160. Worden BD, Parker PG, Pappas PW (2000) Parasites reduce attractiveness and reproductive success in male grain beetles. Anim Behav 59(3):543–550.  https://doi.org/10.1006/anbe.1999.1368 PubMedCrossRefGoogle Scholar
  161. Young TP (1990) Evolution of semelparity in Mount Kenya lobelias. Evol Ecol 4(2):157–171.  https://doi.org/10.1007/BF02270913 CrossRefGoogle Scholar
  162. Zera AJ, Harshman LG (2001) The physiology of life history trade-offs in animals. Annu Rev Ecol Syst 32(1):95–126.  https://doi.org/10.1146/annurev.ecolsys.32.081501.114006 CrossRefGoogle Scholar
  163. Zuk M, Stoehr AM (2002) Immune defense and host life history. Am Nat 160(S4):S9–S22.  https://doi.org/10.1086/342131 PubMedCrossRefGoogle Scholar
  164. Zwaan B, Bijlsma R, Hoekstra RF (1995) Direct selection on life span in Drosophila melanogaster. Evolution 49(4):649–659.  https://doi.org/10.1111/j.1558-5646.1995.tb02301.x PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  • Kristin R. Duffield
    • 1
  • E. Keith Bowers
    • 2
  • Scott K. Sakaluk
    • 1
  • Ben M. Sadd
    • 1
  1. 1.Behavior, Ecology, Evolution & Systematics Section, School of Biological SciencesIllinois State UniversityNormalUSA
  2. 2.Department of Biological Sciences and Edward J. Meeman Biological StationUniversity of MemphisMemphisUSA

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