Metabolism, oxidative stress and territorial behaviour in a female colour polymorphic cichlid fish

详细信息    查看全文

• 作者：Peter D. Dijkstra ; Michele E.R. Pierotti…
• 关键词：Metabolic costs ; Oxidative stress ; Female ; female competition ; Sexual selection ; Cichlid fish ; Lake Victoria
• 刊名：Behavioral Ecology and Sociobiology
• 出版年：2016
• 出版时间：January 2016
• 年：2016
• 卷：70
• 期：1
• 页码：99-109
• 全文大小：517 KB
• 参考文献：Baerends GP, Baerends-van Roon JM (1950) An introduction to the study of the ethology of cichlid fishes. Behav Suppl 1:233–366
  Bagni M, Civitareale C, Priori A, Ballerini A, Finoia M, Brambilla G, Marino G (2007) Pre-slaughter crowding stress and killing procedures affecting quality and welfare in sea bass (Dicentrarchus labrax) and sea bream (Sparus aurata). Aquaculture 263:52–60CrossRef
  Beamonte-Barrientos R, Verhulst S (2013) Plasma reactive oxygen metabolites and non-enzymatic antioxidant capacity are not affected by an acute increase of metabolic rate in zebra finches. J Comp Physiol B 183:675–83PubMed CrossRef
  Berglund A, Bisazza A, Pilastro A (1996) Armaments and ornaments: an evolutionary explanation of traits of dual utility. Biol J Linn Soc 58:385–399CrossRef
  Bittner TD, King RB, Kerfin JM (2002) Effects of body size and melanism on the thermal biology of garter snakes (Thamnophis sirtalis). Copeia 2002:477–482CrossRef
  Borowsky R (1984) The evolutionary genetics of Xiphophorus. In: Turner BJ (ed) Evolutionary genetics of fishes. Plenum Press, New York, pp 235–310CrossRef
  Brambilla G, Civitareale C, Ballerini A et al (2002) Response to oxidative stress as a welfare parameter in swine. Redox Rep 7:159–163PubMed CrossRef
  Briffa M, Sneddon LU (2007) Physiological constraints on contest behaviour. Funct Ecol 21:627–637CrossRef
  Brooks R (2000) Negative genetic correlation between male sexual attractiveness and survival. Nature 406:67–70PubMed CrossRef
  Brown JH, Ross B, McCauley S, Dance S, Taylor AC, Huntingford FA (2003) Resting metabolic rate and social status in juvenile giant freshwater prawns, Macrobrachium rosenbergii. Mar Freshw Behav Physiol 36:31–40CrossRef
  Burton T, Killen SS, Armstrong JD, Metcalfe NB (2011) What causes intraspecific variation in resting metabolic rate and what are its ecological consequences? Proc R Soc Lond B 278:3465–3473CrossRef
  Careau V, Thomas D, Humphries MM, Reale D (2008) Energy metabolism and animal personality. Oikos 117:641–653CrossRef
  Castro N, Ros RFH, Becker K, Oliveira RF (2006) Metabolic costs of aggressive behaviour in the Siamese fighting fish, Betta splendens. Aggress Behav 32:474–480CrossRef
  Chapman LJ, Nordlie FG, Seifert A (2002) Respiratory oxygen consumption among groups of Pseudocrenilabrus multicolor victoriae subjected to different oxygen concentrations during development. J Fish Biol 61:242–251CrossRef
  Cole GL, Endler JA (2015) Variable environmental effects on a multicomponent sexually selected Trait. Am Nat 185:452–468PubMed CrossRef
  Costantini D, Casagrande S, De Filippis S, Brambilla G, Fanfani A, Tagliavini J, Dell'Omo G (2006) Correlates of oxidative stress in wild kestrel nestlings (Falco tinnunculus). J Comp Physiol B 176:329–337PubMed CrossRef
  Costantini D, Monaghan P, Metcalfe NB (2013) Loss of integration is associated with reduced resistance to oxidative stress. J Exp Biol 216:2213–2220PubMed CrossRef
  Cutts CJ, Metcalfe NB, Taylor AC (1998) Aggression and growth depression in juvenile Atlantic salmon: the consequences of individual variation in standard. J Fish Biol 44:1026–1037CrossRef
  Dijkstra PD, Groothuis TGG (2011) Male-male competition as a force in evolutionary diversification: evidence in haplochromine cichlid fish. Int J Evol Biol 2011:689254PubMed PubMedCentral CrossRef
  Dijkstra PD, Hekman R, Schulz RW, Groothuis TGG (2006) Social stimulation, nuptial colouration, androgens and immunocompetence in a sexual dimorphic cichlid fish. Behav Ecol Sociobiol 61:599–609CrossRef
  Dijkstra PD, Lindström J, Metcalfe NB, Hemelrijk CK, Brendel M, Seehausen O, Groothuis TGG (2010) Frequency-dependent social dominance in a color polymorphic cichlid fish. Evolution 64:2797–2807PubMed
  Dijkstra PD, Seehausen O, Groothuis TGG (2005) Direct male-male competition can facilitate invasion of new colour types in Lake Victoria cichlids. Behav Ecol Sociobiol 58:136–143CrossRef
  Dijkstra PD, Seehausen O, Groothuis TGG (2008) Intrasexual competition among females and the stabilization of a conspicuous colour polymorphism in a Lake Victoria cichlid fish. Proc R Soc Lond B 275:519–526CrossRef
  Dijkstra PD, Seehausen O, Metcalfe NB (2013) Metabolic divergence between sibling species of cichlids Pundamilia nyererei and Pundamilia pundamilia. J Fish Biol 82:1975–1989PubMed CrossRef
  Dijkstra PD, van Dijk S, Groothuis TGG, Pierotti MER, Seehausen O (2009) Behavioral dominance between female color morphs of a Lake Victoria cichlid fish. Behav Ecol 20:593–600CrossRef
  Dijkstra PD, Wiegertjes GF, Forlenza M, van der Sluijs I, Hofmann HA, Metcalfe NB, Groothuis TGG (2011) The role of physiology in the divergence of two incipient cichlid species. J Evol Biol 24:2639–2652PubMed CrossRef
  Ducrest A-L, Keller L, Roulin A (2008) Pleiotropy in the melanocortin system, coloration and behavioural syndromes. Trends Ecol Evol 23:502–510PubMed CrossRef
  Emaresi G, Ducrest A-L, Bize P, Richter H, Simon C, Roulin A (2013) Pleiotropy in the melanocortin system: expression levels of this system are associated with melanogenesis and pigmentation in the tawny owl (Strix aluco). Mol Ecol 22:4915–4930PubMed CrossRef
  Endler JA (1980) Natural selection on color patterns in Poecilia reticulata. Evolution 34:76–91CrossRef
  Fan S, Elmer KR, Meyer A (2012) Genomics of adaptation and speciation in cichlid fishes: recent advances and analyses in African and Neotropical lineages. Philos T Roy Soc B 367:385–394CrossRef
  Figueiredo-Silva AC, Saravanan S, Schrama JW, Panserat S, Kaushik S, Geurden I (2013) A comparative study of the metabolic response in rainbow trout and Nile tilapia to changes in dietary macronutrient composition. Br J Nutr 109:816–826PubMed CrossRef
  Finkel T, Holbrook NJ (2000) biology of ageing. Nature 408:239–247PubMed CrossRef
  Fletcher QE, Selman C, Boutin S et al (2013) Oxidative damage increases with reproductive energy expenditure and is reduced by food-supplementation. Evolution 67:1527–1536PubMed PubMedCentral
  Galván I, Gangoso L, Grande JM, Negro JJ, Rodríguez A, Figuerola J, Alonso-Alvarez C (2010) Antioxidant machinery differs between melanic and light nestlings of two polymorphic raptors. PLoS ONE 5, e13369PubMed PubMedCentral CrossRef
  Garratt M, Brooks RC (2012) Oxidative stress and condition-dependent sexual signals: more than just seeing red. Proc R Soc Lond B 279:3121–3130CrossRef
  Genner MJ, Turner GF (2005) The mbuna cichlids of Lake Malawi: a model for rapid speciation and adaptive radiation. Fish Fish 6:1–34CrossRef
  Grantner A, Taborsky M (1998) The metabolic rates associated with resting, and with the performance of agonistic, submissive and digging behaviours in the cichlid fish Neolamprologus pulcher (Pisces: Cichlidae). J Comp Physiol B 427–433
  Gray SM, Dill LM, Tantu FY et al (2008) Environment-contingent sexual selection in a colour polymorphic fish. Proc R Soc Lond B 275:1785–1791CrossRef
  Gray SM, McKinnon JS (2007) Linking color polymorphism maintenance and speciation. Trends Ecol Evol 22:71–79PubMed CrossRef
  Grether GF, Losin N, Anderson CN, Okamoto K (2009) The role of interspecific interference competition in character displacement and the evolution of competitor recognition. Biol Rev Camb Philos 84:617–635CrossRef
  Handelsman CA, Broder ED, Dalton CM, Ruell EW, Myrick CA, Reznick DN, Ghalambor CK (2013) Predator-induced phenotypic plasticity in metabolism and rate of growth: Rapid adaptation to a novel environment. Integr Comp Biol 53:975–988PubMed CrossRef
  Herskin J (1999) Effects of social and visual contact on the oxygen consumption of juvenile sea bass measured by computerized intermittent respirometry. J Fish Biol 55:1075–1085CrossRef
  Horth L (2003) Melanic body colour and aggressive mating behaviour are correlated traits in male mosquitofish (Gambusia holbrooki). Proc R Soc Lond B 270:1033–1040CrossRef
  Huffman LS, Mitchell MM, O’Connell LA, Hofmann HA (2012) Rising StARs: Behavioral, hormonal, and molecular responses to social challenge and opportunity. Horm Behav 61:631–641PubMed CrossRef
  Hughes KA, Houde AE, Price AC, Rodd FH (2013) Mating advantage for rare males in wild guppy populations. Nature 503:108–110PubMed CrossRef
  Kocher TD (2004) Adaptive evolution and explosive speciation: the cichlid fish model. Nat Rev Genet 5:288–298PubMed CrossRef
  Lahti K, Huuskonen H, Laurila A, Piironen J (2002) Metabolic rate and aggressiveness between Brown Trout. Funct Ecol 167–174
  Lande R, Seehausen O, van Alphen JJ (2001) Mechanisms of rapid sympatric speciation by sex reversal and sexual selection in cichlid fish. Genetica 112–113:435–443PubMed CrossRef
  Lehtonen TK (2014) Colour biases in territorial aggression in a Neotropical cichlid fish. Oecologia 175:85–93PubMed CrossRef
  Li Q, Clarke JA, Gao K-Q et al (2014) Melanosome evolution indicates a key physiological shift within feathered dinosaurs. Nature 507:350–353PubMed CrossRef
  Maan ME, Eshuis B, Haesler MP et al (2008) Color polymorphism and predation in a Lake Victoria cichlid fish. Copeia 2008:621–629CrossRef
  Maan ME, Sefc KM (2013) Colour variation in cichlid fish: developmental mechanisms, selective pressures and evolutionary consequences. Semin Cell Dev Biol 24:516–528PubMed PubMedCentral CrossRef
  Magalhaes IS, Mwaiko S, Seehausen O (2010) Sympatric colour polymorphisms associated with nonrandom gene flow in cichlid fish of Lake Victoria. Mol Ecol 19:3285–3300PubMed CrossRef
  Majerus MEN (1998) Melanism. Oxford University Press, Oxford, Evolution in action
  Manceau M, Domingues VS, Mallarino R, Hoekstra HE (2011) The developmental role of Agouti in color pattern evolution. Science 331:1062–1065PubMed CrossRef
  Marras S, Claireaux G, McKenzie DJ, Nelson JA (2010) Individual variation and repeatability in aerobic and anaerobic swimming performance of European sea bass, Dicentrarchus labrax. J Exp Biol 213:26–32PubMed CrossRef
  McCarthy I (2000) Temporal repeatability of relative standard metabolic rate in juvenile Atlantic salmon and its relation to life history variation. J Fish Biol 57:224–238CrossRef
  McKinnon JS, Pierotti MER (2010) Colour polymorphism and correlated characters: genetic mechanisms and evolution. Mol Ecol 19:5101–5125PubMed CrossRef
  McLean CA, Stuart-Fox D (2014) Geographic variation in animal colour polymorphisms and its role in speciation. Biol Rev Camb Philos 89:860–873CrossRef
  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 24:984–996CrossRef
  Metcalfe NB, Taylor AC, Thorpe JE (1995) Metabolic rate, social status and life-history strategies in Atlantic salmon. Anim Behav 49:431–436CrossRef
  Meyer CI, Kaufman R, Cech JJ (2006) Melanin pattern morphs do not differ in metabolic rate: implications for the evolutionary maintenance of a melanophore polymorphism in the green swordtail, Xiphophorus helleri. Naturwissenschaften 93:495–499PubMed CrossRef
  Monaghan P, Metcalfe NB, Torres R (2009) Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation. Ecol Lett 12:75–92PubMed CrossRef
  Pierotti MER, Knight ME, Immler S et al (2008) Individual variation in male mating preferences for female coloration in a polymorphic cichlid fish. Behav Ecol 19:483–488CrossRef
  Pierotti MER, Martín-Fernández JA, Seehausen O (2009) Mapping individual variation in male mating preference space: multiple choice in a color polymorphic cichlid fish. Evolution 63:2372–2388PubMed CrossRef
  Pierotti MER, Seehausen O (2007) Male mating preferences pre-date the origin of a female trait polymorphism in an incipient species complex of Lake Victoria cichlids. J Evol Biol 20:240–248PubMed CrossRef
  Pryke SR (2007) Fiery red heads: female dominance among head color morphs in the Gouldian finch. Behav Ecol 18:621–627CrossRef
  Roberts RB, Ser JR, Kocher TD (2009) Sexual conflict resolved by invasion of a novel sex determiner in Lake Malawi cichlid fishes. Science 326:998–1001PubMed PubMedCentral CrossRef
  Ros AFH, Becker K, Canário AVM, Oliveira RF (2004) Androgen levels and energy metabolism in Oreochromis mossambicus. J Fish Biol 65:895–905CrossRef
  Røskaft E, Järvi T, Bakken M et al (1986) The relationship between social status and resting metabolic rate in great tits (Parus major) and pied flycatchers (Ficedula hypoleuca). Anim Behav 34:838–842CrossRef
  Roulin A (2004) The evolution, maintenance and adaptive function of genetic colour polymorphism in birds. Biol Rev Camb Philos 79:815–848CrossRef
  Saino N, Scatizzi L (1991) Selective aggressiveness and dominance among carrion crows, hooded crows and hybrids. B Zool 58:255–260CrossRef
  Salin K, Auer SK, Rey B, Selman C, Metcalfe NB (2015) Variation in the link between oxygen consumption and ATP production, and its relevance for animal performance. Proc R Soc B 282:20151028
  Salin K, Luquet E, Rey B et al (2012) Alteration of mitochondrial efficiency affects oxidative balance, development and growth in frog (Rana temporaria) tadpoles. J Exp Biol 215:863–869PubMed CrossRef
  Secor SM (2009) Specific dynamic action: a review of the postprandial metabolic response. J Comp Physiol B 179:1–56PubMed CrossRef
  Seebacher F, Ward AJW, Wilson RS (2013) Increased aggression during pregnancy comes at a higher metabolic cost. J Exp Biol 216:771–776PubMed CrossRef
  Seehausen O (1996) Lake Victoria rock cichlids. Taxonomy, ecology and distribution. Cichlid Press, Zevenhuizen, NL
  Seehausen O (2006) African cichlid fish: a model system in adaptive radiation research. Proc R Soc Lond B 273:1987–1998CrossRef
  Seehausen O, Schluter D (2004) Male-male competition and nuptial-colour displacement as a diversifying force in Lake Victoria cichlid fishes. Proc R Soc Lond B 271:1345–1353CrossRef
  Seehausen O, van Alphen JJM, Lande R (1999) Color polymorphism and sex ratio distortion in a cichlid fish as an incipient stage in sympatric speciation by sexual selection. Ecol Lett 2:367–378CrossRef
  Sinervo B, Calsbeek R (2006) The developmental, physiological, neural, and genetical causes and consequences of frequency-dependent selection in the wild. Annu Rev Ecol Evol Syst 37:581–610CrossRef
  Speakman JR, Selman C (2003) Physical activity and resting metabolic rate. Proc Nutr Soc 62:621–634PubMed CrossRef
  Steffensen JF, Johansen K, Bushnell PG (1984) An automated swimming respirometer. Comp Biochem Phys A 79:437–440CrossRef
  Watson P, Lighton JRB (1994) Sexual selection and the energetics of copulatory courtship in the Sierra dome spider, Linyphia litigiosa. Anim Behav 48:615–626CrossRef
  West-Eberhard MJ (1979) Sexual selection, social competition, and evolution. Proc Am Philos Soc 123:222–234
  Wong BBM, Candolin U (2005) How is female mate choice affected by male competition? Biol Rev Camb Philos 80:559–571CrossRef
  Yamamoto T, Ueda H, Higashi S (1998) Correlation among dominance status, metabolic rate and otolith size in masu salmon. J Fish Biol 52:281–290CrossRef
  Zhang C, Song Y, Thompson DA et al (2010) Pineal-specific agouti protein regulates teleost background adaptation. Proc Natl Acad Sci U S A 107:20164–20171PubMed PubMedCentral CrossRef
  
• 作者单位：Peter D. Dijkstra (1) (2)
  Michele E.R. Pierotti (3) (4) (5)
  Ole Seehausen (3) (4)
  Neil B. Metcalfe (1)
  
  1. Institute of Biodiversity, Animal Health and Comparative Medicine, Graham Kerr Building, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, G12 8QQ, UK
  2. Department of Biology, Central Michigan University, Mount Pleasant, MI, USA
  3. Centre of Ecology, Evolution and Biogeochemistry, Eawag Swiss Federal Institute for Aquatic Sciences, CH-6047, Kastanienbaum, Switzerland
  4. Institute of Ecology and Evolution, Division Aquatic Ecology and Evolution, University of Bern, Baltzerstr.6, CH-3012, Bern, Switzerland
  5. Smithsonian Tropical Research Institute, 0843-03092, Panama, Republic of Panama
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Life Sciences
  Behavioural Sciences
  Zoology
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1432-0762

文摘

Intrasexual selection on body coloration is thought to play an important role in the evolution of colour polymorphism, but its physiological underpinnings have received limited attention. In the colour polymorphic cichlid Neochromis omnicaeruleus, three fully sympatric female colour morphs—a plain morph (P) and two conspicuously coloured blotched morphs, black-and-white blotched (WB) and orange blotched (OB)—differ in agonistic behaviour. We compared routine metabolic rate (when females were housed in social isolation), short-term energetic costs of interacting with a same-colour rival housed in an adjacent transparent chamber and oxidative stress between the three female colour morphs. WB females had a lower routine metabolic rate compared with the other colour morphs. WB females also had a lower active metabolic rate during inter-female interactions than OB females, while OB females used more oxygen per unit aggressive act than the other two colour morphs. However, there were no consistent differences in oxidative stress between the three morphs. Concerted divergence in colour, behaviour and metabolism might contribute to the evolution of these polymorphisms in sympatry. Keywords Metabolic costs Oxidative stress Female-female competition Sexual selection Cichlid fish Lake Victoria