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The Role of Oxidative Stress and Hormesis in Shaping Reproductive Strategies

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Oxidative Stress and Hormesis in Evolutionary Ecology and Physiology

Abstract

The cost of reproduction is a central paradigm of life history theory. It states that high investment in current reproduction reduces survival or future fecundity. Reproduction is a demanding phase of animals’ lives, since they must produce, and, in species with parental care, protect and provision, their young. In sexually reproducing species, considerable resources are also invested in mate choice strategies, which combine to shape the cost of reproduction. We currently know very little about how costs of reproduction are actually incurred, since the majority of studies have focussed on the ultimate outcomes rather than the proximate mechanisms. It has been suggested that oxidative stress may be one key cellular mechanism underlying the costs of reproduction. This chapter examines how the need to manage oxidative stress has possibly influenced the evolution of reproductive strategies, from the tactics adopted to find a suitable mate to how much effort parents put in offspring rearing. This chapter also discusses the possible prominent role of hormesis in determining the extent to which (1) reproductive activity may be stressful or not and (2) mild stress may stimulate reproductive performance.

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References

  • Abuelo A, Pérez-Santos M, Hernández J, Castillo C (2014) Effect of colostrum redox balance on the oxidative status of calves during the first 3 months of life and the relationship with passive immune acquisition. Veter J 199:295–299

    CAS  Google Scholar 

  • Ahmadi MR, Bazyar AA, Safi S, Ytrestøyl T, Bjerkeng B (2006) Effects of dietary astaxanthin supplementation on reproductive characteristics of rainbow trout (Oncorhynchus mykiss). J Appl Ichthyol 22:388–394

    CAS  Google Scholar 

  • Aitken RJ, Roman SD (2008) Antioxidant systems and oxidative stress in the testes. Oxid Medic Cell Long 1:15–24

    Google Scholar 

  • Aitken RJ, Clarkson JS, Fishel S (1989) Generation of reactive oxygen species, lipid peroxidation, and human sperm function. Biol Reprod 40:183–197

    Google Scholar 

  • Alberts SC, Altmann J, Wilson ML (1996) Mate guarding constrains foraging activity of male baboons. Anim Behav 51:1269–1277

    Google Scholar 

  • Alberts SC, Watts H, Altmann J (2003) Queuing and queue-jumping: long-term patterns of reproductive skew in male savannah baboons, Papio cynocephalus. Anim Behav 65:821–840

    Google Scholar 

  • Alcock J (2009) Animal behavior, 9th edn. Sinauer Associates, Sunderland

    Google Scholar 

  • 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 7:363–368

    Google Scholar 

  • Angilletta MJ Jr, Sears MW (2000) The metabolic cost of reproduction in an oviparous lizard. Funct Ecol 14:39–45

    Google Scholar 

  • Arenas-Ríos E, León-Galván MA, Mercado PE, Rosado A (2005) Superoxide dismutase, catalase, and glutathione peroxidase during epididymal maturation and prolonged storage of spermatozoa in the Mexican big-eared bat (Corynorhinus mexicanus). Can J Zool 83:1556–1565

    Google Scholar 

  • Attisano A, Moore AJ, Moore PJ (2012) Reproduction-longevity trade-offs reflect diet, not adaptation. J Evol Biol 25:873–880

    PubMed  CAS  Google Scholar 

  • Ayyanath M-M, Cutler GC, Scott-Dupree CD, Sibley PK (2013) Transgenerational shifts in reproduction hormesis in green peach aphid exposed to low concentrations of imidacloprid. PLoS ONE 8:e74532

    PubMed Central  PubMed  CAS  Google Scholar 

  • Barske J, Schlinger BA, Wikelski M, Fusani L (2011) Female choice for male motor skills. Proc R Soc Lond B 278:3523–3528

    Google Scholar 

  • Baumber J, Ball BA, Gravance CG, Medina V, Davies-Morel MCG (2000) The effect of reactive oxygen species on equine sperm motility, viability, acrosomal integrity, mitochondrial membrane potential, and membrane lipid peroxidation. J Androl 21:895–902

    PubMed  CAS  Google Scholar 

  • Beaulieu M, Reichert S, Le Maho Y, Ancel A, Criscuolo F (2011) Oxidative status and telomere length in a long-lived bird facing a costly reproductive event. Funct Ecol 25:577–585

    Google Scholar 

  • Béguel J-P, Huvet A, Quillien V, Lambert C, Fabioux C (2013) Study of the antioxidant capacity in gills of the Pacific oyster Crassostrea gigas in link with its reproductive investment. Comp Biochem Physiol Part C 157:63–71

    Google Scholar 

  • Bell G (1980) The costs of reproduction and their consequences. Am Nat 116:45–77

    Google Scholar 

  • Bergeron P, Careau V, Humphries MM, Reale D, Speakman JR, Garant D (2011) The energetic and oxidative costs of reproduction in a free-ranging rodent. Funct Ecol 761(25):1063–1071

    Google Scholar 

  • Berglund A, Rosenqvist G, Svensson I (1986) Mate choice, fecundity and sexual dimorphism in two pipefish species (Syngnathidae). Behav Ecol Sociobiol 19:301–307

    Google Scholar 

  • Bertrand S, Alonso-Alvarez C, Devevey G, Faivre B, Prost J, Sorci G (2006) Carotenoids modulate the trade-off between egg production and resistance to oxidative stress in zebra finches. Oecologia 147:576–584

    PubMed  Google Scholar 

  • Bilodeau J-F, Blanchette S, Cormier N, Sirard M-A (2002) Reactive oxygen species-mediated loss of bovine serm motility in egg yolk Tris extender: protection by pyruvate, metal chelators and bovine liver or oviductal fluid catalase. Theriogenol 57:1105–1122

    CAS  Google Scholar 

  • Birkhead TR, Møller AP (1993) Sexual selection and the temporal separation of reproductive events: sperm storage data from reptiles, birds and mammals. Biol J Linn Soc 50:295–311

    Google Scholar 

  • Bize P, Devevey G, Monaghan P, Doligez B, Christe P (2008) Fecundity and survival in relation to resistance to oxidative stress in a free-living bird. Ecology 89:2584–2593

    PubMed  Google Scholar 

  • Blount JD, Surai PF, Houston DC, Møller AP (2002a) Patterns of yolk enrichment with dietary carotenoids in gulls: the roles of pigment acquisition and utilization. Funct Ecol 16:445–453

    Google Scholar 

  • Blount JD, Surai PF, Nager RG, Houston DC, Møller AP, Trewby ML, Kennedy MW (2002b) Carotenoids and egg quality in the lesser black-backed gull Larus fuscus: a supplemental feeding study of maternal effects. Proc R Soc Lond B 269:29–36

    CAS  Google Scholar 

  • Boldt J, Schuel H, Schuel R, Dandeckar PV, Troll W (1981) Reaction of sperm with egg-derived hydrogen peroxide helps prevent polyspermy during fertilization in the sea urchin. Gamete Res 4:365–377

    CAS  Google Scholar 

  • Bonisoli-Alquati A, Møller AP, Rudolfsen G, Saino N, Caprioli M, Ostermiller S, Mousseau TA (2011) The effects of radiation on sperm swimming behavior depend on plasma oxidative status in the barn swallow (Hirundo rustica). Comp Biochem Physiol Part A 159:105–112

    Google Scholar 

  • Bouwhuis S, Charmantier A, Verhulst S, Sheldon BC (2010) Trans-generational effects on ageing in a wild bird population. J Evol Biol 23:636–642

    PubMed  CAS  Google Scholar 

  • Brown JL (1987) Helping and communal breeding in birds. Princeton University Press, Princeton

    Google Scholar 

  • Brown-Borg HM (2007) Hormonal regulation of longevity in mammals. Ageing Res Rev 6:28–45

    PubMed Central  PubMed  CAS  Google Scholar 

  • Byers J, Hebets E, Podos J (2010) Female mate choice based upon male motor performance. Anim Behav 79:771–778

    Google Scholar 

  • Calabrese EJ (2001a) Estrogen and related compounds: biphasic dose responses. Crit Rev Toxicol 31:503–515

    PubMed  CAS  Google Scholar 

  • Calabrese EJ (2001b) Androgens: biphasic dose responses. Crit Rev Toxicol 31:517–522

    PubMed  CAS  Google Scholar 

  • Calabrese EJ, Baldwin LA (2003) The hormetic dose response model is more common than the threshold model in toxicology. Toxicol Sci 71:414–428

    Google Scholar 

  • Calabrese EJ, Blain R (2005) The occurrence of hormetic dose responses in the toxicological literature, the hormesis database: an overview. Toxicol Appl Pharmacol 202:289–301

    PubMed  CAS  Google Scholar 

  • Cardoso VV, Ferreira MP, Montagner JM, Fernandez CG, Moreira JC, Oliveira AK (2002) The effects of constant and alternating temperatures on the reproductive potential, life span, and life expectancy of Anastrepha fraterculus (Wiedemann) (Diptera: Tephritidae). Braz J Biol 62:775–786

    PubMed  CAS  Google Scholar 

  • Casagrande S, Dell’Omo G, Costantini D, Tagliavini J, Groothuis T (2011) Variation of a carotenoid-based trait in relation to oxidative stress and endocrine status during the breeding season in the Eurasian kestrel: a multi-factorial study. Comp Biochem Physiol Part A 160:16–26

    CAS  Google Scholar 

  • Christie P, Glaizot O, Strepparava N, Devevey G, Fumagalli L (2012) Twofold cost of reproduction: an increase in parental effort leads to higher malarial parasitaemia and to a decrease in resistance to oxidative stress. Proc R Soc Lond B 279:1142–1149

    Google Scholar 

  • Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, Princeton

    Google Scholar 

  • Clutton-Brock T, Huchard E (2013) Social competition and its consequences in female mammals. J Zool 289:151–171

    Google Scholar 

  • Coburn M, Schuel H, Troll W (1981) A hydrogen peroxide block to polyspermy in the sea urchin Arbacia punctulata. Dev Biol 84:235–238

    PubMed  CAS  Google Scholar 

  • Collins AM, Williams V, Evans JD (2004) Sperm storage and antioxidative enzyme expression in the honey bee, Apis mellifera. Ins Mol Biol 13:141–146

    CAS  Google Scholar 

  • Costantini D (2008) Oxidative stress in ecology and evolution: lessons from avian studies. Ecol Lett 11:1238–1251

    PubMed  Google Scholar 

  • Costantini D (2010a) Complex trade-offs in the pigeon (Columba livia): egg antioxidant capacity and female serum oxidative status in relation to diet quality. J Comp Physiol B 180:731–739

    PubMed  CAS  Google Scholar 

  • Costantini D (2010b) Effects of diet quality on serum oxidative status and body mass in male and female pigeons during reproduction. Comp Biochem Physiol Part A 156:294–299

    Google Scholar 

  • Costantini D, Carello L, Fanfani A (2010a) Relationships among oxidative status, breeding conditions and life-history traits in free-living great tits Parus major and common starlings Sturnus vulgaris. Ibis 152:793–802

    Google Scholar 

  • Costantini D, Rowe M, Butler MW, McGraw KJ (2010b) From molecules to living systems: historical and contemporary issues in oxidative stress and antioxidant ecology. Funct Ecol 24:950–959

    Google Scholar 

  • Costantini D, Marasco V, Møller AP (2011) A meta-analysis of glucocorticoids as modulators of oxidative stress in vertebrates. J Comp Physiol B 181:447–456

    PubMed  CAS  Google Scholar 

  • Cram DL (2013) Causes and consequences of oxidative stress in a cooperatively breeding bird. Ph.D. Dissertation, University of Exeter, Exeter

    Google Scholar 

  • van de Crommenacker J, Komdeur J, Richardson DS (2011) Assessing the cost of helping: the roles of body condition and oxidative balance in the Seychelles warbler (Acrocephalus sechellensis). PLoS ONE 6:e26423

    PubMed Central  PubMed  Google Scholar 

  • Crump ML (1974) Reproductive strategies in a tropical anuran community. Misc Publs Mus Nat Hist Univ Kans 61:1–68

    Google Scholar 

  • Cutler GC, Ramanaidu K, Astatkie T, Isman MB (2009) Green peach aphid, Myzus persicae (Hemiptera: Aphididae), reproduction during exposure to sublethal concentrations of imidacloprid and azadirachtin. Pest Manag Sci 65:205–209

    CAS  Google Scholar 

  • Daan S, Deerenberg C, Dijkstra C (1996) Increased daily work precipitates natural death in the kestrel. J Anim Ecol 65:539–544

    Google Scholar 

  • Dean R, Bonsall MB, Pizzari T (2007) Aging and sexual conflict. Science 316:383–384

    PubMed  CAS  Google Scholar 

  • Dean R, Cornwallis CK, Løvlie H, Worley K, Richardson DS, Pizzari T (2010) Male reproductive senescence causes potential for sexual conflict over mating. Curr Biol 20:1192–1196

    PubMed  CAS  Google Scholar 

  • Deerenberg C, Pen I, Dijkstra C, Arkies BJ, Visser GH, Daan S (1995) Parental energy expenditure in relation to manipulated brood size in the European kestrel, Falco tinnunculus. Zoology 99:38–47

    Google Scholar 

  • Doucet SM, Montgomerie R (2003) Multiple sexual ornaments in satin bowerbirds: ultraviolet plumage and bowers signal different aspects of male quality. Behav Ecol 14:503–509

    Google Scholar 

  • Drent RH, Daan S (1980) The prudent parent: energetic adjustments in avian breeding. Ardea 68:225–252

    Google Scholar 

  • Eaton TH Jr (1941) Notes on the life history of Dendrobates auratus. Copeia 1941:93–95

    Google Scholar 

  • Eskes T, Haanen C (2007) Why do women live longer than men? Eur J Obstet Gynecol Reprod Biol 133:126–133

    PubMed  Google Scholar 

  • Fletcher QE, Selman C, Boutin S, McAdam AG, Woods SB, Seo AY, Leeuwenburgh C, Speakman JR, Humphries MM (2013) Oxidative damage increases with reproductive energy expenditure and is reduced by food-supplementation. Evolution 67:1527–1536

    PubMed  Google Scholar 

  • Fox CW, Dingle H (1994) Dietary mediation of maternal age effects on offspring performance in a seed beetle (Coleoptera: Bruchidae). Funct Ecol 8:600–606

    Google Scholar 

  • Fu P, Neff BD, Gross MR (2001) Tactic-specific success in sperm competition. Proc R Soc Lond B 268:1105–1112

    CAS  Google Scholar 

  • Fujihara N, Howarth B (1978) Lipid peroxidation in fowl spermatozoa. Poult Sci 57:1766–1768

    PubMed  CAS  Google Scholar 

  • Fusani L, Giordano M, Day L, Schlinger B (2007) High-speed video analysis reveals individual variability in the courtship displays of male golden-collared manakins. Ethology 113:964–972

    Google Scholar 

  • Garratt M, Vasilaki A, Stockley P, McArdle F, Jackson M, Hurst JL (2011) Is oxidative stress a physiological cost of reproduction? An experimental test in house mice. Proc R Soc Lond B 278:1098–1106

    Google Scholar 

  • Garratt M, McArdle F, Stockley P, Vasilaki A, Beynon RJ, Jackson MJ, Hurst JL (2012) Tissue-dependent changes in oxidative damage with male reproductive effort in house mice. Funct Ecol 26:423–433

    Google Scholar 

  • Garratt M, Pichaud N, King EDA, Brooks RC (2013) Physiological adaptations to reproduction I. Experimentally increasing litter size enhances aspects of antioxidant defence but does not cause oxidative damage in mice. J Exp Biol 216:2879–2888

    PubMed  CAS  Google Scholar 

  • Giesy JP, Pierens SL, Snyder EM, Miles-Richardson S, Kramer VJ, Snyder SA, Nichols KM, Villeneuve DA (2000) Effects of 4-nonylphenol on fecundity and biomarkers of estrogenicity in fathead minnows (Pimephales promelas). Environm Toxicol Chem 19:1368–1377

    CAS  Google Scholar 

  • Giron D, Casas J (2003) Mothers reduce egg provisioning with age. Ecol Lett 6:273–277

    Google Scholar 

  • Godeas C, Tramer F, Micali F, Soranzo MR, Sandri G, Panfili E (1997) Distribution and possible novel role of phospholipid hydroperoxide glutathione peroxidase in rat epididymal spermatozoa. Biol Reprod 57:1502–1508

    PubMed  CAS  Google Scholar 

  • Griffith SC, Owens IPF, Thuman KA (2002) Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11:2195–2212

    PubMed  CAS  Google Scholar 

  • Guindre-Parker S, Baldo S, Gilchrist HG, MacDonald CA, Harris CM, Love OP (2013) The oxidative costs of territory quality and offspring provisioning. J Evol Biol 26:2558–2565

    PubMed  CAS  Google Scholar 

  • Gupta NP, Kumar R (2002) Lycopene therapy in idiopathic male infertility-a preliminary report. Int Urol Nephrol 34:369–372

    PubMed  CAS  Google Scholar 

  • Gwynne DT (1981) Sexual difference theory: Mormon crickets show role reversal in mate choice. Science 213:779–780

    PubMed  CAS  Google Scholar 

  • Hammond KA (1997) Adaptation of the maternal intestine during lactation. J Mammary Gland Biol Neoplasia 2:243–252

    PubMed  CAS  Google Scholar 

  • Hatamoto LK, Sobrinho CAB, Nichi M, Barnabe VH, Barnabe RC, Cortada CNM (2006) Effects of dexamethasone treatment (to mimic stress) and vitamin E oral supplementation on the spermiogram and on seminal plasma spontaneous lipid peroxidation and antioxidant enzyme activities in dogs. Theriogenol 66:1610–1614

    CAS  Google Scholar 

  • Heinsohn R, Cockburn A (1994) Helping is costly to young birds in cooperatively breeding white-winged choughs. Proc R Soc Lond B 256:293–298

    Google Scholar 

  • Heinz GH, Hoffman DJ, Klimstra JD, Stebbins KR (2010) Enhanced reproduction in mallards fed a low level of methylmercury: an apparent case of hormesis. Environ Toxicol Chem 29:650–653

    PubMed  CAS  Google Scholar 

  • Heinz GH, Hoffman DJ, Klimstra JD, Stebbins KR, Kondrad SL, Erwin CA (2012) Hormesis associated with a low dose of methylmercury injected into mallard eggs. Arch Environ Contam Toxicol 62:141–144

    PubMed  CAS  Google Scholar 

  • Heiss RS, Schoech SJ (2012) Oxidative cost of reproduction is sex specific and correlated with reproductive effort in a cooperatively breeding bird, the Florida scrub jay. Physiol Biochem Zool 85:499–503

    PubMed  Google Scholar 

  • Helfenstein F, Losdat S, Møller AP, Blount JD, Richner H (2010) Sperm of colourful males are better protected against oxidative stress. Ecol Lett 13:213–222

    PubMed  Google Scholar 

  • Heller K-G, Fleischmann P, Lutz-Röder A (2000) Carotenoids in the spermatophores of bushcrickets (Orthoptera: Ephippigerinae). Proc R Soc Lond B 267:1905–1908

    CAS  Google Scholar 

  • Hoogland JL (1995) The black-tailed prairie dog. Chicago University Press, Chicago

    Google Scholar 

  • Hu H, Wang M, Zhan XA, Li X, Zhao RQ (2011) Effect of different selenium sources on productive performance, serum and milk Se concentrations, and antioxidant status of sows. Biol Trace Elem Res 142:471–480

    PubMed  CAS  Google Scholar 

  • Jamieson CD, Santer B (2003) Maternal aging in the univoltine freshwater copepod Cyclops kolensis: variation in egg sizes, egg development times, and naupliar development times. Hydrobiologia 510:75–81

    Google Scholar 

  • Jolly A, Pride RE (1999) Troop histories and range inertia of Lemur catta at Berenty, Madagascar: a 33-year perspective. Int J Primatol 20:359–373

    Google Scholar 

  • Kervinen M, Alatalo R, Lebigre C, Siitari H, Soulsbury C (2012) Determinants of yearling male lekking effort and mating success in black grouse (Tetrao tetrix). Behav Ecol 23:1209–1217

    Google Scholar 

  • King EDA, Garratt M, Brooks R (2013) Manipulating reproductive effort leads to changes in female reproductive scheduling but not oxidative stress. Ecol Evol 3:4161–4171

    Google Scholar 

  • Komdeur J (2001) Mate guarding in the Seychelles warbler is energetically costly and adjusted to paternity risk. Proc R Soc Lond B 268:2103–2111

    CAS  Google Scholar 

  • Kumagai H, Chaipan Y (2004) Changes of vitamin E status of periparturient dairy cows and newborn calves. Anim Sci J 75:541–547

    CAS  Google Scholar 

  • Kuningas M, Altmäe S, Uitterlinden AG, Hofman A (2011) The relationship between fertility and lifespan in humans. Age 33:615–622

    PubMed Central  PubMed  Google Scholar 

  • de Lamirande E, Gagnon C (1992) Reactive oxygen species and human spermatozoa. I. Effect on the motility of intact spermatozoa and on sperm axonemes. J Androl 13:368–378

    PubMed  Google Scholar 

  • de Lamirande E, Gagnon C (1993) Human sperm hyperactivation and capacitation as parts of an oxidative process. Free Rad Biol Medic 14:157–166

    Google Scholar 

  • de Lamirande E, Jiang H, Zini A, Kodama H, Gagnon C (1997) Reactive oxygen species and sperm physiology. Rev Reprod 2:48–54

    PubMed  Google Scholar 

  • Lansing AI (1947) A transmissible, cumulative, and reversible factor in aging. J Geront 2:228–239

    PubMed  CAS  Google Scholar 

  • Law R (1979) The cost of reproduction in annual meadow grass. Am Nat 113:3–16

    Google Scholar 

  • Lindén M, Møller AP (1989) Cost of reproduction and covariation of life history traits in birds. Trends Ecol Evol 4:367–371

    PubMed  Google Scholar 

  • Locatello L, Rasotto MB, Evans JP, Pilastro A (2006) Colourful male guppies produce faster and more viable sperm. J Evol Biol 19:1595–1602

    PubMed  CAS  Google Scholar 

  • López-Martínez G, Hahn DA (2012) Short-term anoxic conditioning hormesis boosts antioxidant defenses, lowers oxidative damage following irradiation and enhances male sexual performance in the Caribbean fruit fly, Anastrepha suspensa. J Exp Biol 215:2150–2161

    PubMed  Google Scholar 

  • Losdat S, Helfenstein F, Gaude B, Richner H (2011a) Reproductive effort transiently reduces antioxidant capacity in a wild bird. Behav Ecol 22:1218–1226

    Google Scholar 

  • Losdat S, Helfenstein F, Saladin V, Richner H (2011b) Higher in vitro resistance to oxidative stress in extra-pair offspring. J Evol Biol 24:2525–2530

    PubMed  CAS  Google Scholar 

  • Lozano GA, Lank DB, Addison B (2013) Immune and oxidative stress trade-offs in four classes of ruffs (Philomachus pugnax) with different reproductive strategies. Can J Zool 91:212–218

    CAS  Google Scholar 

  • Lund E, Arnesen E, Borgan J-K (1990) Pattern of childbearing and mortality in married women-a national prospective study from Norway. J Epidem Comm Health 44:237–240

    CAS  Google Scholar 

  • Markó G, Costantini D, Michl G, Török J (2011) Oxidative damage and plasma antioxidant capacity in relation to body size, age, male sexual traits and female reproductive performance in the collared flycatcher (Ficedula albicollis). J Comp Physiol B 181:73–81

    PubMed  Google Scholar 

  • Martin-Coello J, Dopazo H, Arbiza L, Ausió J, Roldan ERS, Gomendio M (2009) Sexual selection drives weak positive selection in protamine genes and high promoter divergence, enhancing sperm competitiveness. Proc R Soc Lond B 276:2427–2436

    CAS  Google Scholar 

  • McArdle PF, Pollin TI, O’Connell JR, Sorkin JD, Agarwala R, Schaffer AA, Streeten EA, King TM, Shuldiner AR, Mitchell BD (2006) Does having children extend life span? A genealogical study of parity and longevity in the Amish. J Gerontol Biol Sci Med Sci 61:190–195

    Google Scholar 

  • McGraw KJ, Adkins-Regan E, Parker RS (2005) Maternally derived carotenoid pigments affect offspring survival, sex ratio, and sexual attractiveness in a colorful songbird. Naturwissenschaften 92:375–380

    PubMed  CAS  Google Scholar 

  • Maklakov AA, Immler S, Løvlie H, Flis I, Friberg U (2012) The effect of sexual harassment on lethal mutation rate in female Drosophila melanogaster. Proc R Soc Lond B 280:20121874

    Google Scholar 

  • Martin TE (2004) Avian life-history evolution has an eminent past: does it have a bright future? Auk 121:289–301

    Google Scholar 

  • Metcalfe NB, Alonso-Alvarez C (2010) Oxidative stress as a life-history constraint: the role of reactive oxygen species in shaping phenotypes from conception to death. Funct Ecol 24:984–996

    Google Scholar 

  • Metcalfe NB, Monaghan P (2013) Does reproduction cause oxidative stress? An open question. Trends Ecol Evol 28:347–350

    PubMed  Google Scholar 

  • Miller GM, Watson SA, McCormick MI, Munday PL (2013) Increased CO2 stimulates reproduction in a coral reef fish. Global Change Biol 19:3037–3045

    Google Scholar 

  • Mills SC, Hazard L, Lancaster L, Mappes T, Miles D, Oksanen TA, Sinervo B (2008) Gonadotropin hormone modulation of testosterone, immune function, performance, and behavioral trade-offs among male morphs of the lizard Uta stansburiana. Am Nat 171:339–357

    PubMed  Google Scholar 

  • Monaghan P, Nager RG (1997) Why don’t birds lay more eggs? Trends Ecol Evol 12:270–274

    PubMed  CAS  Google Scholar 

  • Monaghan P, Nager RG, Houston DC (1998) The price of eggs: increased investment in egg production reduces offspring rearing capacity of parents. Proc R Soc Lond B 265:1731–1735

    Google Scholar 

  • Monaghan P, Metcalfe NB, Torres R (2009) Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol Lett 12:75–92

    Google Scholar 

  • Monaghan P, Heidinger BJ, D’Alba L, Evans NP, Spencer KA (2012) For better or worse: reduced adult lifespan following early-life stress is transmitted to breeding partners. Proc R Soc Lond B 279:709–714

    Google Scholar 

  • Morse JG, Zareh N (1991) Pesticide-induced hormoligosis of citrus thrips (Thysanoptera: Thripidae) fecundity. J Econ Entomol 84:1169–1174

    CAS  Google Scholar 

  • Nager R, Monaghan P, Houston DC (2000) Within clutch trade-off between the number and quality of eggs: experimental study in gulls. Ecology 81:1339–1350

    Google Scholar 

  • Nager R, Monaghan P, Houston DC (2001) The cost of egg production: increased egg production reduces future fitness in gulls. J Avian Biol 32:159–166

    Google Scholar 

  • Nedelcu AM (2005) Sex as a response to oxidative stress: stress genes co-opted for sex. Proc R Soc Lond B 272:1935–1940

    CAS  Google Scholar 

  • Nedelcu AM, Michod RE (2003) Sex as a response to oxidative stress: the effect of antioxidants on sexual induction in a facultatively sexual lineage. Biol Lett 270:136–139

    Google Scholar 

  • Nedelcu AM, Marcu O, Michod RE (2004) Sex as a response to oxidative stress: a twofold increase in cellular reactive oxygen species activates sex genes. Proc R Soc Lond B 271:1591–1596

    CAS  Google Scholar 

  • Nilsson J-Å (2002) Metabolic consequences of hard work. Proc R Soc Lond B 269:1735–1739

    Google Scholar 

  • Noguera JC, Dean R, Isaksson C, Velando A, Pizzari T (2012) Age-specific oxidative status and the expression of pre- and postcopulatory sexually selected traits in male red junglefowl, Gallus gallus. Ecol Evol 2:2155–2167

    PubMed Central  PubMed  Google Scholar 

  • Nussey DH, Pemberton JM, Pilkington JG, Blount JD (2009) Life history correlates of oxidative damage in a free-living mammal population. Funct Ecol 23:809–817

    Google Scholar 

  • Olsson M, Healey M, Perrin C, Wilson M, Tobler M (2012) Sex-specific SOD levels and DNA damage in painted dragon lizards (Ctenophorus pictus). Oecologia 170:917–924

    PubMed  Google Scholar 

  • Orrell KS, Jenssen TA (2002) Male mate choice by the lizard Anolis carolinensis: a preference for novel females. Anim Behav 63:1091–1102

    Google Scholar 

  • Palombit RA, Seyfarth RM, Cheney DL (1997) The adaptive value of ‘friendships’ to female baboons: experimental and observational evidence. Anim Behav 54:599–614

    PubMed  Google Scholar 

  • Pamilo P (1991) Life span of queens in the ant Formica exsecta. Ins Soc 38:111–119

    Google Scholar 

  • Paquet M, Covas R, Chastel O, Parenteau C, Doutrelant C (2013) Maternal effects in relation to helper presence in the cooperatively breeding sociable weaver. PLoS ONE 8:e59336

    PubMed Central  PubMed  CAS  Google Scholar 

  • Parkhurst BR, Bradshaw AS, Forte JL, Wright GP (1981) The chronic toxicity to Daphnia magna of acridine, a representative azaarene present in synthetic fossil fuel products and wastewaters. Environ Poll 24:21–30

    CAS  Google Scholar 

  • Peters A, Denk AG, Delhey K, Kempenaers B (2004) Carotenoid-based bill colour as an indicator of immunocompetence and sperm performance in male mallards. J Evol Biol 17:1111–1120

    PubMed  CAS  Google Scholar 

  • Pichaud N, Garratt M, Ballard JWO, Brooks RC (2013) Physiological adaptations to reproduction II. Mitochondrial adjustments in livers of lactating mice. J Exp Biol 216:2889–2895

    PubMed  CAS  Google Scholar 

  • Pike TW, Blount JD, Lindström J, Metcalfe NB (2010) Dietary carotenoid availability, sexual signaling and functional fertility in sticklebacks. Biol Lett 6:191–193

    PubMed Central  PubMed  CAS  Google Scholar 

  • Pitcher TE, Rodd FH, Rowe L (2007) Sexual colouration and sperm traits in guppies. J Fish Biol 70:165–177

    Google Scholar 

  • Pizzari T, Dean R, Pacey A, Moore H, Bonsall MB (2008) The evolutionary ecology of pre- and post-meiotic sperm senescence. Trends Ecol Evol 23:131–140

    PubMed  Google Scholar 

  • Preston BT, Saint-Jalme M, Hingrat Y, Lacroix F, Sorci G (2011) Sexually extravagant males age more rapidly. Ecol Lett 14:1017–1024

    PubMed  Google Scholar 

  • Priest NK, Mackowiak B, Promislow DEL (2002) The role of parental age effects on the evolution of aging. Evolution 56:927–935

    PubMed  Google Scholar 

  • Reed TE, Kruuk LEB, Wanless S, Frederiksen M, Cunningham EJA, Harris MP (2008) Reproductive senescence in a long-lived seabird: rates of decline in late life performance are associated with varying costs of early reproduction. Am Nat 171:89–101

    Google Scholar 

  • Reglero MM, Taggart MA, Castellanos P, Mateo R (2009) Reduced sperm quality in relation to oxidative stress in red deer from a lead mining area. Envir Poll 157:2209–2215

    CAS  Google Scholar 

  • Reznick D, Bryant M, Holmes D (2006) The evolution of senescence and post-reproductive lifespan in guppies (Poecilia reticulata). PLoS Biol 4:e7

    PubMed Central  PubMed  Google Scholar 

  • Ridgway MS (1988) Developmental stage of offspring and brood defence in smallmouth bass (Micropterus dolomieu). Can J Zool 66:1722–1728

    Google Scholar 

  • Rizzo A, Ceci E, Pantaleo M, Mutinati M, Spedicato M, Minoia G, Sciorsci RL (2013) Evaluation of blood and milk oxidative status during early postpartum of dairy cows. Animal 7:118–123

    PubMed  CAS  Google Scholar 

  • Rodríguez-Graña L, Calliari D, Tiselius P, Hansen BW, Sköld HN (2010) Gender-specific ageing and non-Mendelian inheritance of oxidative damage in marine copepods. Mar Ecol Prog Ser 401:1–13

    Google Scholar 

  • Roff DA (2002) Life history evolution. Sinauer Associates, Sunderland

    Google Scholar 

  • Rosvall KA (2011) Intrasexual competition in females: evidence for sexual selection? Behav Ecol 22:1131–1140

    PubMed Central  PubMed  Google Scholar 

  • Royle NJ, Surai PF, McCartney RJ, Speake BK (1999) Parental investment and egg yolk lipid composition in gulls. Funct Ecol 13:298–306

    Google Scholar 

  • Royle NJ, Surai PF, Hartley IR (2003) The effect of variation in dietary intake on maternal deposition of antioxidants in zebra finch eggs. Funct Ecol 17:472–481

    Google Scholar 

  • Rowe M, McGraw KJ (2008) Carotenoids in the seminal fluid of wild birds: interspecific variation in fairy-wrens. Condor 110:694–700

    Google Scholar 

  • Saeki Y, Kruse KC, Switzer PV (2005) Physiological costs of mate guarding in the Japanese beetle (Popillia japonica Newman). Ethology 111:863–877

    Google Scholar 

  • Salomons HM (2009) Fighting for fitness: telomeres, oxidative stress and life history trade-offs in a colonial corvid. Ph.D. Thesis, University of Groningen, Groningen, The Netherlands

    Google Scholar 

  • Santos ESA, Nakagawa S (2012) The costs of parental care: a meta-analysis of the trade-off between parental effort and survival in birds. J Evol Biol 25:1911–1917

    PubMed  CAS  Google Scholar 

  • Schreck CB (2010) Stress and fish reproduction: the roles of allostasis and hormesis. Gener Comp Endocrinol 165:549–556

    CAS  Google Scholar 

  • Sclar DC, Gerace D, Cranshaw WS (1998) Observation of population increases and injury by spider mites (Acari: Tetranychidae) on ornamental plants treated with imidacloprid. J Econ Entomol 91:250–255

    CAS  Google Scholar 

  • Selman C, Blount JD, Nussey DH, Speakman J (2012) Oxidative damage, ageing, and life history evolution: where now? Trends Ecol Evol 10:570–577

    Google Scholar 

  • Sharp SP, Clutton-Brock TH (2011) Competition, breeding success and ageing rates in female meerkats. J Evol Biol 24:1756–1762

    PubMed  CAS  Google Scholar 

  • Shuster SM (1989) Male alternative reproductive strategies in a marine isopod crustacean (Paracerceis sculpta): the use of genetic markers to measure differences in the fertilization success among alpha, beta, and gamma-males. Evolution 43:1683–1689

    Google Scholar 

  • Shuster SM (1992) The reproductive behaviour of alpha, beta, and gamma morphs in Paracerceis sculpta: a marine isopod crustacean. Behaviour 121:231–258

    Google Scholar 

  • Shuster SM, Wade MJ (1991) Equal mating success among male reproductive strategies in a marine isopod. Nature 350:608–610

    Google Scholar 

  • Siitari H, Alatalo RV, Halme P, Buchanan KL, Kilpimaa J (2007) Color signals in the black grouse (Tetrao tetrix): signal properties and their condition dependency. Am Nat 169:S81–S92

    PubMed  Google Scholar 

  • Sikka SC (2001) Relative impact of oxidative stress on male reproductive function. Curr Med Chem 8:851–862

    PubMed  CAS  Google Scholar 

  • Siva-Jothy MT (2000) The young sperm gambit. Ecol Lett 3:172–174

    Google Scholar 

  • Snell TW, King CE (1977) Lifespan and fecundity patterns in rotifers: the cost of reproduction. Evolution 31:882–890

    Google Scholar 

  • Solomon NG, French JA (1997) Cooperative breeding in mammals. Cambridge University Press, Cambridge

    Google Scholar 

  • Speakman JR (2008) The physiological costs of reproduction in small mammals. Phil Trans R Soc B 363:375–398

    PubMed Central  PubMed  Google Scholar 

  • Spencer KA, Heidinger BJ, D’Alba LB, Evans N, Monaghan P (2010) Then versus now: effect of developmental and current environmental conditions on incubation effort in birds. Behav Ecol 21:999–1004

    Google Scholar 

  • Stacey PB, Koenig WD (1990) Cooperative breeding in birds: long-term studies of ecology and behavior. Cambridge University Press, Cambridge

    Google Scholar 

  • Stahlschmidt ZR, Lourdais O, Lorioux S, Butler MW, Davis JR, Salin K, Voituron Y, DeNardo DL (2013) Morphological and physiological changes during reproduction and their relationships to reproductive performance in a capital breeder. Physiol Biochem Zool 86:398–409

    PubMed  CAS  Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

    Google Scholar 

  • Stephens PA, Boyd IL, McNamara JM, Houston AI (2009) Capital breeding and income breeding: their meaning, measurement, and worth. Ecology 90:2057–2067

    PubMed  Google Scholar 

  • Stier A, Reichert S, Massemin S, Bize P, Criscuolo F (2012) Constraint and cost of oxidative stress on reproduction: correlative evidence in laboratory mice and review of the literature. Front Zool 9:37

    PubMed Central  PubMed  Google Scholar 

  • Surai PF (2002) Natural antioxidants in avian nutrition and reproduction. Nottingham University Press, Nottingham

    Google Scholar 

  • Surai PF, Kutz E, Wishart GJ, Noble RC, Speake BK (1997) The relationship between the dietary provision of α-tocopherol and the concentration of this vitamin in the semen of chicken: effects on lipid composition and susceptibility to peroxidation. J Reprod Fert 110:47–51

    CAS  Google Scholar 

  • Tarín JJ, Pérez-Albalá S, Cano A (2000) Consequences on offspring of abnormal function in ageing gametes. Human Reprod Update 6:532–549

    Google Scholar 

  • Tarín JJ, Gomez-Piquer V, Raussell F, Navarro S, Hermenegildo C, Cano A (2005) Delayed motherhood decreases life expectancy of mouse offspring. Biol Reprod 72:1336–1343

    PubMed  Google Scholar 

  • Travers M, Clinchy M, Zanette L, Boonstra R, Williams TD (2010) Indirect predator effects on clutch size and the cost of egg production. Ecol Lett 13:980–988

    PubMed  Google Scholar 

  • Velando A, Noguera JC, Drummond H, Torres R (2011) Senescent males carry premutagenic lesions in sperm. J Evol Biol 24:693–697

    PubMed  CAS  Google Scholar 

  • Wagner RH, Helfenstein F, Danchin E (2004) Female choice of young sperm in a genetically monogamous bird. Proc R Soc Lond B 271:S134–S137

    Google Scholar 

  • Wang Y, Salmon AB, Harshman LG (2001) A cost of reproduction: oxidative stress susceptibility is associated with increased egg production in Drosophila melanogaster. Exp Geront 36:1349–1359

    CAS  Google Scholar 

  • Wang AH, Wu JC, Yu YS, Liu JL, Yu JF, Wang MY (2005) Selective insecticide induced stimulation on fecundity and biochemical changes in Tryporyza incertulas (Lepidoptera: Pyralidae). J Econ Entomol 4:1143–1149

    Google Scholar 

  • Weirich GF, Collins AM, Williams VP (2002) Antioxidant enzymes in the honey bee, Apis mellifera. Apidol 33:3–14

    CAS  Google Scholar 

  • Westneat DF, Stewart IRK (2003) Extra-pair paternity in birds: causes, correlates, and conflict. Annu Rev Ecol Syst 34:365–396

    Google Scholar 

  • Wiersma P, Selman C, Speakman JR, Verhulst S (2004) Birds sacrifice oxidative protection for reproduction. Biol Lett 271:360–363

    Google Scholar 

  • Williams GC (1966) Natural selection, the costs of reproduction, and a refinement of Lack’s principle. Am Nat 100:687–690

    Google Scholar 

  • Wilson SM, Gravel M-A, Mackie TA, Willmore WG, Cooke SJ (2012) Oxidative stress associated with parental care in smallmouth bass (Micropterus dolomieu). Comp Biochem Physiol Part A 162:212–218

    CAS  Google Scholar 

  • Wilson SM, Taylor JJ, Mackie TA, Patterson DA, Cooke SJ, Willmore WG (2014) Oxidative stress in Pacific salmon (Oncorhynchus spp.) during spawning migration. Physiol Biochem Zool (in press)

    Google Scholar 

  • Wishart GJ (1984) Effects of lipid peroxide formation in fowl semen on sperm motility, ATP content and fertilizing ability. J Reprod Fertil 71:113–118

    PubMed  CAS  Google Scholar 

  • Wu SH, Oldfield JE, Whanger PD, Weswig PH (1973) Effect of selenium, vitamin E, and antioxidants on testicular function in rats. Biol Reprod 8:625–629

    PubMed  CAS  Google Scholar 

  • Yang D-B, Xu Y-C, Wang D-H, Speakman JR (2013) Effects of reproduction on immuno-suppression and oxidative damage, and hence support or otherwise for their roles as mechanisms underpinning life history trade-offs, are tissue and assay dependent. J Exp Biol 216:4242–4250

    PubMed  CAS  Google Scholar 

  • Young AJ, Carlson AA, Monfort SL, Russell AF, Bennett NC, Clutton-Brock T (2006) Stress and the suppression of subordinate reproduction in cooperatively breeding meerkats. Proc Natl Acad Sci USA 103:12005–12010

    PubMed Central  PubMed  CAS  Google Scholar 

  • Young AM (1979) Arboreal movement and tadpole-carrying behaviour of Dendrobates pumilio Schmidt (Dendrobatidae) in Northeastern Costa Rica. Biotropica 11:238–239

    Google Scholar 

  • Yu Y, Shen G, Zhu H, Lu Y (2010) Imidacloprid-induced hormesis on the fecundity and juvenile hormone levels of the green peach aphid Myzus persicae (Sulzer). Pest Biochem Physiol 98:238–242

    CAS  Google Scholar 

  • Xu Y-C, Yang D-B, Speakman JR, Wang D-H (2014) Oxidative stress in response to natural and experimentally elevated reproductive effort is tissue dependent. Funct Ecol (in press)

    Google Scholar 

  • Zanuncio JC, Jusselino-Filho P, Ribeiro RC, Zanuncio TV, Ramalho Fde S, Serrão JE (2011) Hormetic responses of a stinkbug predator to sublethal doses of pyrethroid. Bull Environ Contam Toxicol 87:608–614

    PubMed  CAS  Google Scholar 

  • Zini A, de Lamirande E, Gagnon C (1995) Low levels of nitric oxide promote human sperm capacitation in vitro. J Androl 16:424–431

    PubMed  CAS  Google Scholar 

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  1. Department of Biology, University of Antwerp, Universiteitsplein House No. 1, 2610, Wilrijk, Antwerp, Belgium

    David Costantini

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Costantini, D. (2014). The Role of Oxidative Stress and Hormesis in Shaping Reproductive Strategies. In: Oxidative Stress and Hormesis in Evolutionary Ecology and Physiology. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-54663-1_7

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