Inbreeding depression in intraspecific metabolic scaling

in Animal Biology
Restricted Access
Get Access to Full Text
Rent on DeepDyve

Have an Access Token?



Enter your access token to activate and access content online.

Please login and go to your personal user account to enter your access token.



Help

Have Institutional Access?



Access content through your institution. Any other coaching guidance?



Connect

Metabolic scaling (i.e., the relationship between the size and metabolic rate of organisms) has been suggested to explain a large variety of biological patterns from individual growth to species diversity. However, considerable disagreement remains regarding the underlying causes of metabolic scaling patterns, and what these patterns are. As in all biology, understanding metabolic scaling will require understanding its evolution by natural selection. We searched for evidence of natural selection on metabolic scaling indirectly by manipulating the genetic quality of male and female Drosophila montana flies with induced mutations and inbreeding, building on the notion that mutations and inbreeding will cause predictable changes in characters under directional selection. Irradiation-induced mutations had no effect on the examined traits, most likely because of purging at an early stage. However, inbreeding increased the energy use of larger females, suggesting that selection has favoured low metabolic scaling in females. Inbreeding did not affect metabolic scaling of males. Together, our results suggest that natural selection on metabolic scaling acts differently on the sexes, depending on the relative importance of body size and energetic efficiency to individual fitness. The results call attention to the important notion that size-specific energy use can be an evolutionarily malleable trait.

Inbreeding depression in intraspecific metabolic scaling

in Animal Biology

Sections

References

AgutterP.WheatleyD. (2004) Metabolic scaling: consensus or controversy? Theor. Biol. Med. Model.113.

ArtachoP.NespoloR.F. (2009) Natural selection reduces energy metabolism in the garden snail, Helix aspersa (Cornu aspersum). Evolution631044-1050.

BanavarJ.R.MosesM.E.BrownJ.H.DamuthJ.RinaldoA.SiblyR.M.MaritanA. (2010) A general basis for quarter power scaling in animals. Proc. Nat. Acad. Sci.10715816-15820.

BerriganD.PartridgeL. (1997) Influence of temperature and activity on the metabolic rate of adult Drosophila melanogaster. Comp. Biochem. Physiol.118A1301-1307.

BlanckenhornW.U. (2000) The evolution of body size: what keeps organisms small? Q. Rev. Biol.75385-407.

BokmaF. (2004) Evidence against universal metabolic allometry. Funct. Ecol.18184-187.

BoratyńskiZ.KoskelaE.MappesT.SchroderusE. (2012) Quantitative genetics and fitness effects of basal metabolism. Evol. Ecol.27301-314.

CapelliniI.VendittiC.BartonR. (2010) Phylogeny and metabolic scaling in mammals. Ecology912783-2793.

CharlesworthD.CharlesworthB. (1987) Inbreeding depression and its evolutionary consequences. Annu. Rev. Ecol. Syst.18237-268.

DeroseM.A.RoffD.A. (1999) A comparison of inbreeding depression in life-history and morphological traits in animals. Evolution531288-1292.

EggsetC.K.HansenT.F.Le RouzicA.BolstadG.H.RozenqvistG.PélabonC. (2012) Artificial selection on allometry: change in elevation but not slope. J. Evol. Biol.25938-948.

Eyre-WalkerA.KeightleyP.D. (2007) The distribution of fitness effects of new mutations. Nat. Rev. Genet.8610-618.

FalconerD.S.MackayT.F.C. (1996) Introduction to Quantitative Genetics. PearsonHarlow.

GilloolyJ.F.BrownJ.H.WestG.B.SavageV.M.CharnovE.L. (2001) Effects of size and temperature on metabolic rate. Science2932248-2251.

GlazierD.S. (2005) Beyond the ‘3/4-power law’: variation in intra- and interspecific scaling of metabolic rate in animals. Biol. Rev.801-52.

GlazierD.S. (2009) Activity affects intraspecific body-size scaling of metabolic rate in ectothermic animals. J. Comp. Physiol. B.179821-828.

HayesA.F.MatthesJ. (2009) Computational procedures for probing interactions in OLS and logistic regression: SPSS and SAS implementations. Behav. Res. Methods41924-936.

HendrixL.J.CarterM.W.ScottD.T. (1982) Covariance analyses with heterogeneity of slopes in fixed models. Biometrics38641-650.

HochachkaP.W.SomeroG.N. (2002) Biochemical Adaptation: Mechanism and Process in Physiological Evolution. Oxford University PressOxford.

HoikkalaA.KlappertK.MazziD. (2005) Factors affecting male song evolution in Drosophila montana. Curr. Top. Dev. Biol.67225-250.

HoněkA. (1993) Intraspecific variation in body size and fecundity in insects – a general relationship. Oikos66483-492.

IsaacN.J.B.CarboneC. (2010) Why are metabolic scaling exponents so controversial? Quantifying variance and testing hypotheses. Ecol. Lett.13728-735.

KarasovW.H.del RioC.M. (2007) Physiological Ecology: How Animals Process Energy Nutrients and Toxins. Princeton University PressPrinceton.

KetolaT.KotiahoJ.S. (2009) Inbreeding, energy use and condition. J. Evol. Biol.22770-781.

KetolaT.KotiahoJ.S. (2012) Inbreeding depression in the effects of body mass on energy use. Biol. J. Linn. Soc.105309-317.

KetolaT.BoratyńskiZ.KotiahoJ.S. (2013) Manipulating genetic architecture to reveal fitness relationships. Proceedings of Peerage of Science (accepted).

KöhlerM.Moyà-SolàS. (2009) Physiological and life history strategies of a fossil large mammal in a resource-limited environment. Proc. Nat. Acad. Sci.10620354-20358.

KonarzewskiM.DiamondJ. (1995) Evolution of basal metabolic rate and organ masses in laboratory mice. Evolution491239-1248.

KozlowskiJ.WeinerJ. (1997) Interspecific allometries are by-products of body size optimization. Am. Nat.149352-380.

KristensenT.N.SørensenP.KruhofferM.PedersenK.S.LoeschckeV. (2005) Genome-wide analysis on inbreeding effects on gene expression in Drosophila melanogaster. Genetics171157-167.

MattilaA.L.K.DuployA.KirjokangasM.LehtonenR.RastasP.HanskiI. (2012) High genetic load in an old isolated butterfly population. Proc. Nat. Acad. Sci.109E2496-E2505.

ParsonsP.A. (2005) Environments and evolution: interactions between stress, resource inadequacy and energetic efficiency. Biol. Rev.80589-610.

PedersenK.S.KristensenT.N.LoeschckeV.PetersenB.O.DuusJ.O.NielsenN.Chr MalmendalA. (2008) Metabolomic signatures of inbreeding in benign and stressful environments in Drosophila melanogaster. Genetics1801235-1243.

PekkalaN.PuurtinenM.KotiahoJ.S. (2009) Sexual selection for genetic quality: disentangling the roles of male and female behaviour. Anim. Behav.781357-1363.

PurvisA.HarveyP.H. (1997) Evolutionary ecology – the right size for a mammal. Nature386332-333.

StraussK.ReinholdK. (2010) Scaling of metabolic rate in the lesser wax moth Achroia grisella does not fit the 3/4-power law and shows significant sex differences. Physiol. Entomol.3559-63.

Van VoorhiesW.A.KhazaeliA.A.CurtsingerJ.W. (2004) Lack of correlation between body mass and metabolic rate in Drosophila melanogaster. J. Insect Physiol.50445-453.

WhiteC.R.CasseyP.BlackburnT.M. (2007) Allometric exponents do not support a universal metabolic allometry. Ecology88315-323.

WhitfieldJ. (2004) Ecology’s big, hot idea. PLoS Biol.2e440.

Figures

  • View in gallery

    Overview of the breeding design used to produce the experimental groups. Squares denote males and circles denote females. Filled symbols indicate that individuals are potential carriers of mutations induced through induced mutations of the parental (P) generation. This mating scheme (both groups) was replicated 31 times. Individuals of the F3 generation were the measured subjects in the study. The expected genotype frequencies at autosomal loci in the F3 generation are given below the figure, assuming zero inbreeding coefficient for the parental generation. Denotes pairing the male with an unrelated female within the same treatment (Induced mutations or Control).

  • View in gallery

    Effects of body mass (log10 mg) and inbreeding on resting metabolic rate (log10 ml CO2 h−1) of male (panel A) and female (panel B) Drosophila montana. The solid line and filled circles indicate inbred (f = 0.25) individuals, and the dashed line and open circles indicate non-inbred individuals (irradiation treatment groups were pooled for figure). The space between the two vertical dashed lines in panel B corresponds to the body mass interval within which inbred and control groups do not differ in their metabolic rates significantly (P>0.05) in their metabolic rates. In males inbred and control treatments did not differ in metabolic rates and thus vertical lines were not drawn.

Index Card

Content Metrics

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 23 23 6
Full Text Views 0 0 0
PDF Downloads 0 0 0
EPUB Downloads 0 0 0