Multiple Paternity Benefits Female Marbled Salamanders by Increasing Survival of Progeny to Metamorphosis

Croshaw, Dean A.; Pechmann, Joseph H. K.; Glenn, Travis C.; Hebets, ed., Eileen

doi:10.1111/eth.12597

Multiple Paternity Benefits Female Marbled Salamanders by Increasing Survival of Progeny to Metamorphosis

Journal Article · Tue Mar 21 00:00:00 EDT 2017 · Ethology

DOI:https://doi.org/10.1111/eth.12597· OSTI ID:1401896

Croshaw, Dean A. ^[1]; Pechmann, Joseph H. K. ^[2]; Glenn, Travis C. ^[3]; Hebets, ed., Eileen

Department of Biological Sciences Florida Gulf Coast University Fort Myers FL USA, Savannah River Ecology Laboratory Drawer E Aiken SC USA
Department of Biological Sciences Western Carolina University Cullowhee NC USA
Department of Environmental Health Science University of Georgia Athens GA USA

Abstract

Multiple paternity occurs in most species and animal groups that have been studied. Because mating involves fitness costs to individual females, theory predicts that polyandrous females gain greater fitness benefits than costs, allowing the behavior to be maintained. Genetic, rather than material, benefits often occur in species where males provide females with little more than sperm and seminal fluid. We compared fitness correlates of single‐ and double‐sire clutches from female marbled salamanders ( Ambystoma opacum ) at the egg, hatchling, and metamorph stages of offspring development. Because clutches were collected from experimental breeding groups, strict paternity exclusion of offspring using microsatellite data allowed us to categorize each clutch as having either one or two fathers. Early offspring viability and size of hatchlings were not different between single‐ and multiple‐paternity clutches. Larvae from the two clutch types were allowed to develop together in field enclosures until metamorphosis. Although there was no difference in size at metamorphosis, survival to metamorphosis was significantly higher in multiple‐paternity clutches (44% vs. 40%) suggesting a benefit for females. The results were consistent with genetic benefits, although maternal effects could not be ruled out. The data did not support predictions of the genetic bet‐hedging and good sperm hypotheses for genetic benefits of polyandry.

View Accepted Manuscript (Publisher)

Sponsoring Organization:: USDOE

Grant/Contract Number:: FC09-96SR18546

OSTI ID:: 1401896

Journal Information:: Ethology, Journal Name: Ethology Journal Issue: 4 Vol. 123; ISSN 0179-1613

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: Country unknown/Code not available

Language:: English

References (53)

Female sperm storage in amphibians Sever, David M. Journal of Experimental Zoology, Vol. 292, Issue 2 https://doi.org/10.1002/jez.1152	journal	December 2001
Morphology and evolutionary implications of the annual cycle of secretion and sperm storage in spermathecae of the salamanderAmbystoma opacum (Amphibia: Ambystomatidae) Sever, David M.; Krenz, John D.; Johnson, Kristin M. Journal of Morphology, Vol. 223, Issue 1 https://doi.org/10.1002/jmor.1052230106	journal	January 1995
Why do female Gunnison's prairie dogs copulate with more than one male? Hoogland, John L. Animal Behaviour, Vol. 55, Issue 2 https://doi.org/10.1006/anbe.1997.0575	journal	February 1998
The evolution of polyandry: multiple mating and female fitness in insects Arnqvist, Göran; Nilsson, Tina Animal Behaviour, Vol. 60, Issue 2 https://doi.org/10.1006/anbe.2000.1446	journal	August 2000
Multiple paternity, sperm storage, and reproductive success of female and male painted turtles ( Chrysemys picta ) in nature Pearse, Devon; Janzen, Fred; Avise, John Behavioral Ecology and Sociobiology, Vol. 51, Issue 2 https://doi.org/10.1007/s00265-001-0421-7	journal	January 2002
Temporal patterns in reproduction may explain variationin mating frequencies in the green-veined white butterfly Pieris napi Välimäki, Panu; Kaitala, Arja; Kokko, Hanna Behavioral Ecology and Sociobiology, Vol. 61, Issue 1 https://doi.org/10.1007/s00265-006-0240-y	journal	August 2006
Fallow deer polyandry is related to fertilization insurance Briefer, Elodie F.; Farrell, Mary E.; Hayden, Thomas J. Behavioral Ecology and Sociobiology, Vol. 67, Issue 4 https://doi.org/10.1007/s00265-013-1485-x	journal	January 2013
Multiple insemination increases reproductive success of female Montandon's newt ( Triturus montandoni , Caudata, Salamandridae) Osikowski, Artur; Rafin´ski, Jan Behavioral Ecology and Sociobiology, Vol. 49, Issue 2-3 https://doi.org/10.1007/s002650000277	journal	January 2001
Isolation and characterization of microsatellite DNA loci from Ambystoma salamanders Croshaw, Dean A.; Schable, Nancy A.; Peters, Maureen B. Conservation Genetics, Vol. 6, Issue 3 https://doi.org/10.1007/s10592-005-4989-8	journal	May 2005
Variation in polyandry and its fitness consequences among populations of the red flour beetle, Tribolium castaneum Pai, Aditi; Feil, Stacy; Yan, Guiyun Evolutionary Ecology, Vol. 21, Issue 5 https://doi.org/10.1007/s10682-006-9146-4	journal	January 2007
Spermatophores of the salamander Ambystoma texanum Russell, Lonnie D.; Brandon, Ronald A.; Zalisko, Edward J. Tissue and Cell, Vol. 13, Issue 3 https://doi.org/10.1016/0040-8166(81)90031-8	journal	January 1981
Sexual selection Andersson, Malte; Iwasa, Yoh Trends in Ecology & Evolution, Vol. 11, Issue 2 https://doi.org/10.1016/0169-5347(96)81042-1	journal	February 1996
Multiple paternity as genetic bet-hedging in female sierra dome spiders, Linyphia litigiosa (Linyphiidae) Watson, Paul J. Animal Behaviour, Vol. 41, Issue 2 https://doi.org/10.1016/S0003-3472(05)80486-5	journal	February 1991
Sexual conflict resulting from adaptations to sperm competition Stockley, P. Trends in Ecology & Evolution, Vol. 12, Issue 4 https://doi.org/10.1016/S0169-5347(97)01000-8	journal	April 1997
Genetic evidence for sexual selection in black ratsnakes, Elaphe obsoleta Blouin-Demers, Gabriel; Gibbs, H. Lisle; Weatherhead, Patrick J. Animal Behaviour, Vol. 69, Issue 1 https://doi.org/10.1016/j.anbehav.2004.03.012	journal	January 2005
Multiple mating increases female fitness in Drosophila simulans Taylor, Michelle L.; Wigmore, Clare; Hodgson, David J. Animal Behaviour, Vol. 76, Issue 3 https://doi.org/10.1016/j.anbehav.2008.05.015	journal	September 2008
Adaptively flexible polyandry Gowaty, Patricia Adair Animal Behaviour, Vol. 86, Issue 5 https://doi.org/10.1016/j.anbehav.2013.08.015	journal	November 2013
Polyandry is context dependent but not convenient in a mostly monandrous wasp Boulton, Rebecca A.; Shuker, David M. Animal Behaviour, Vol. 112 https://doi.org/10.1016/j.anbehav.2015.12.001	journal	February 2016
Direct costs and benefits of multiple mating: Are high female mating rates due to ejaculate replenishment? Worthington, Amy M.; Kelly, Clint D. Behavioural Processes, Vol. 124 https://doi.org/10.1016/j.beproc.2015.12.009	journal	March 2016
Comparing the performance of analytical techniques for genetic parentage of half-sib progeny arrays Croshaw, Dean A.; Peters, Maureen B.; Glenn, Travis C. Genetics Research, Vol. 91, Issue 5 https://doi.org/10.1017/S0016672309990231	journal	October 2009
Why do female adders copulate so frequently? Madsen, Thomas; Shine, Richard; Loman, Jon Nature, Vol. 355, Issue 6359 https://doi.org/10.1038/355440a0	journal	January 1992
Intra-sexual selection in Drosophila Bateman, A. J. Heredity, Vol. 2, Issue 3 https://doi.org/10.1038/hdy.1948.21	journal	December 1948
Post-mating sexual selection increases lifetime fitness of polyandrous females in the wild Fisher, Diana O.; Double, Michael C.; Blomberg, Simon P. Nature, Vol. 444, Issue 7115 https://doi.org/10.1038/nature05206	journal	November 2006
Statistical confidence for likelihood‐based paternity inference in natural populations Marshall, T. C.; Slate, J.; Kruuk, L. E. B. Molecular Ecology, Vol. 7, Issue 5 https://doi.org/10.1046/j.1365-294x.1998.00374.x	journal	May 1998
A "Good-Sperm" Model Can Explain the Evolution of Costly Multiple Mating by Females Yasui, Yukio The American Naturalist, Vol. 149, Issue 3 https://doi.org/10.1086/286006	journal	March 1997
Polyandry in grain beetles, Tenebrio molitor, leads to greater reproductive success: material or genetic benefits? Worden, B. D. Behavioral Ecology, Vol. 12, Issue 6 https://doi.org/10.1093/beheco/12.6.761	journal	November 2001
Genetic analysis of the mating system and opportunity for sexual selection in northern water snakes (Nerodia sipedon) Prosser, M. R. Behavioral Ecology, Vol. 13, Issue 6 https://doi.org/10.1093/beheco/13.6.800	journal	November 2002
Effects of simultaneous polyandry on offspring fitness in an African tree frog Byrne, Phillip G.; Whiting, Martin J. Behavioral Ecology, Vol. 22, Issue 2 https://doi.org/10.1093/beheco/arq153	journal	January 2011
Relatedness, body size and paternity in the alpine newt, Triturus alpestris Garner, Trenton W. J.; Schmidt, Benedikt R. Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 270, Issue 1515 https://doi.org/10.1098/rspb.2002.2284	journal	March 2003
Condition dependence of reproductive strategy and the benefits of polyandry in a viviparous lizard Eizaguirre, Christophe; Laloi, David; Massot, Manuel Proceedings of the Royal Society B: Biological Sciences, Vol. 274, Issue 1608 https://doi.org/10.1098/rspb.2006.3740	journal	November 2006
Mating portfolios: bet-hedging, sexual selection and female multiple mating Garcia-Gonzalez, Francisco; Yasui, Yukio; Evans, Jonathan P. Proceedings of the Royal Society B: Biological Sciences, Vol. 282, Issue 1798 https://doi.org/10.1098/rspb.2014.1525	journal	January 2015
She gets many and she chooses the best: polygynandry in Salamandrina perspicillata (Amphibia: Salamandridae) Rovelli, Valentina; Randi, Ettore; Davoli, Francesca Biological Journal of the Linnean Society, Vol. 116, Issue 3 https://doi.org/10.1111/bij.12613	journal	July 2015
Bet hedging via multiple mating: A meta-analysis: BET HEDGING AND MULTIPLE MATING Holman, Luke Evolution, Vol. 70, Issue 1 https://doi.org/10.1111/evo.12822	journal	December 2015
Bet-hedging as a mechanism for the evolution of polyandry, revisited: POLYANDRY AS BET-HEDGING Yasui, Yukio; Garcia-Gonzalez, Francisco Evolution, Vol. 70, Issue 2 https://doi.org/10.1111/evo.12847	journal	January 2016
Polyandry Promotes Enhanced Offspring Survival in Decorated Crickets Ivy, Tracie M.; Sakaluk, Scott K. Evolution, Vol. 59, Issue 1 https://doi.org/10.1111/j.0014-3820.2005.tb00902.x	journal	January 2005
Quantifying sexual selection: a comparison of competing indices with mating system data from a terrestrially breeding salamander: INDICES FOR MEASURING SEXUAL SELECTION Croshaw, Dean A. Biological Journal of the Linnean Society, Vol. 99, Issue 1 https://doi.org/10.1111/j.1095-8312.2009.01337.x	journal	December 2009
Fitness benefits of polyandry for experienced females: BREEDING EXPERIENCE AND POLYANDRY Whittingham, L. A.; Dunn, P. O. Molecular Ecology, Vol. 19, Issue 11 https://doi.org/10.1111/j.1365-294X.2010.04640.x	journal	April 2010
Multiple Mating Increases Fecundity, Fertility and Relative Clutch Mass in the Female Leopard Gecko (Eublepharis macularius) LaDage, Lara D.; Gutzke, William H. N.; Simmons, Richard A. Ethology, Vol. 114, Issue 5 https://doi.org/10.1111/j.1439-0310.2008.01495.x	journal	May 2008
Why do females mate multiply? A review of the genetic benefits Jennions, Michael D.; Petrie, Marion Biological Reviews, Vol. 75, Issue 1 https://doi.org/10.1111/j.1469-185X.1999.tb00040.x	journal	February 2000
Remarkable Amphibian Biomass and Abundance in an Isolated Wetland: Implications for Wetland Conservation Gibbons, J. Whitfield; Winne, Christopher T.; Scott, David E. Conservation Biology, Vol. 20, Issue 5 https://doi.org/10.1111/j.1523-1739.2006.00443.x	journal	October 2006
Advantages of Multiple Matings to Females: a test of the Infertility Hypothesis Using Lizards Olsson, Mats; Shine, Richard Evolution, Vol. 51, Issue 5 https://doi.org/10.1111/j.1558-5646.1997.tb01491.x	journal	October 1997
Remating in Drosophila Melanogaster: are Indirect Benefits Condition Dependent? Long, Tristan A. F.; Pischedda, Alison; Rice, William R. Evolution, Vol. 64, Issue 9 https://doi.org/10.1111/j.1558-5646.2010.00997.x	journal	September 2010
The more the better - polyandry and genetic similarity are positively linked to reproductive success in a natural population of terrestrial salamanders (Salamandra salamandra) Caspers, Barbara A.; Krause, E. Tobias; Hendrix, Ralf Molecular Ecology, Vol. 23, Issue 1 https://doi.org/10.1111/mec.12577	journal	November 2013
Female multiple mating for fertility assurance in red flour beetles ( Tribolium castaneum ) Pai, Aditi; Bennett, Lauren; Yan, Guiyun Canadian Journal of Zoology, Vol. 83, Issue 7 https://doi.org/10.1139/z05-073	journal	July 2005
A test of the genetic compatibility hypothesis with tree swallows, Tachycineta bicolor Barber, Colleen A.; Edwards, Mandy J.; Robertson, Raleigh J. Canadian Journal of Zoology, Vol. 83, Issue 7 https://doi.org/10.1139/z05-091	journal	July 2005
The Evolution of Polyandry: Sperm Competition, Sperm Selection, and Offspring Viability Simmons, Leigh W. Annual Review of Ecology, Evolution, and Systematics, Vol. 36, Issue 1 https://doi.org/10.1146/annurev.ecolsys.36.102403.112501	journal	December 2005
Multiple mating by females is not dependent on body size in the salamander Desmognathus ochrophaeus Shillington, Cara; Verrell, Paul Amphibia-Reptilia, Vol. 17, Issue 1 https://doi.org/10.1163/156853896X00261	journal	January 1996
Genetic and potential non-genetic benefits increase offspring fitness of polyandrous females in non-resource based mating system Kekäläinen, Jukka; Rudolfsen, Geir; Janhunen, Matti BMC Evolutionary Biology, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2148-10-20	journal	January 2010
True polyandry and pseudopolyandry: why does a monandrous fly remate? Fisher, David N.; Doff, Rowan J.; Price, Tom A. R. BMC Evolutionary Biology, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2148-13-157	journal	January 2013
Carolina bay wetlands: Unique habitats of the southeastern United States Sharitz, Rebecca R. Wetlands, Vol. 23, Issue 3 https://doi.org/10.1672/0277-5212(2003)023[0550:CBWUHO]2.0.CO;2	journal	September 2003
The Effect of Larval Density on Adult Demographic Traits in Ambystoma Opacum Scott, David E. Ecology, Vol. 75, Issue 5 https://doi.org/10.2307/1937462	journal	July 1994
Effects of Larval Density in Ambystoma Opacum: An Experiment Large-Scale Field Enclosures Scott, David E. Ecology, Vol. 71, Issue 1 https://doi.org/10.2307/1940269	journal	February 1990
Estimating Fitness: A Comparison of Body Condition Indices Jakob, Elizabeth M.; Marshall, Samuel D.; Uetz, George W. Oikos, Vol. 77, Issue 1 https://doi.org/10.2307/3545585	journal	October 1996

Similar Records

Male body size predicts reproductive success but not within-clutch paternity patterns in gopher tortoises (Gopherus polyphemus)

Journal Article · Wed Jul 18 20:00:00 EDT 2018 · Journal of Heredity · OSTI ID:1828596

EFFECT OF PATERNAL IRRADIATION ON 154 DAY WEIGHT IN SWINE

Journal Article · Fri Nov 30 23:00:00 EST 1962 · Genetics (U.S.) · OSTI ID:4721707

Multiple Paternity Benefits Female Marbled Salamanders by Increasing Survival of Progeny to Metamorphosis

Citation Formats

References (53)

Similar Records

Related Subjects