Multiple Paternity Benefits Female Marbled Salamanders by Increasing Survival of Progeny to Metamorphosis
Abstract
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 goodmore »
- Authors:
-
- 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
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1401896
- Grant/Contract Number:
- DE‐FC09‐96SR18546
- Resource Type:
- Publisher's Accepted Manuscript
- Journal Name:
- Ethology
- Additional Journal Information:
- Journal Name: Ethology Journal Volume: 123 Journal Issue: 4; Journal ID: ISSN 0179-1613
- Publisher:
- Wiley-Blackwell
- Country of Publication:
- Country unknown/Code not available
- Language:
- English
Citation Formats
Croshaw, Dean A., Pechmann, Joseph H. K., Glenn, Travis C., and Hebets, ed., Eileen. Multiple Paternity Benefits Female Marbled Salamanders by Increasing Survival of Progeny to Metamorphosis. Country unknown/Code not available: N. p., 2017.
Web. doi:10.1111/eth.12597.
Croshaw, Dean A., Pechmann, Joseph H. K., Glenn, Travis C., & Hebets, ed., Eileen. Multiple Paternity Benefits Female Marbled Salamanders by Increasing Survival of Progeny to Metamorphosis. Country unknown/Code not available. https://doi.org/10.1111/eth.12597
Croshaw, Dean A., Pechmann, Joseph H. K., Glenn, Travis C., and Hebets, ed., Eileen. Tue .
"Multiple Paternity Benefits Female Marbled Salamanders by Increasing Survival of Progeny to Metamorphosis". Country unknown/Code not available. https://doi.org/10.1111/eth.12597.
@article{osti_1401896,
title = {Multiple Paternity Benefits Female Marbled Salamanders by Increasing Survival of Progeny to Metamorphosis},
author = {Croshaw, Dean A. and Pechmann, Joseph H. K. and Glenn, Travis C. and Hebets, ed., Eileen},
abstractNote = {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.},
doi = {10.1111/eth.12597},
journal = {Ethology},
number = 4,
volume = 123,
place = {Country unknown/Code not available},
year = {Tue Mar 21 00:00:00 EDT 2017},
month = {Tue Mar 21 00:00:00 EDT 2017}
}
https://doi.org/10.1111/eth.12597
Web of Science
Works referenced in this record:
Mating portfolios: bet-hedging, sexual selection and female multiple mating
journal, January 2015
- Garcia-Gonzalez, Francisco; Yasui, Yukio; Evans, Jonathan P.
- Proceedings of the Royal Society B: Biological Sciences, Vol. 282, Issue 1798
Genetic analysis of the mating system and opportunity for sexual selection in northern water snakes (Nerodia sipedon)
journal, November 2002
- Prosser, M. R.
- Behavioral Ecology, Vol. 13, Issue 6
Morphology and evolutionary implications of the annual cycle of secretion and sperm storage in spermathecae of the salamanderAmbystoma opacum (Amphibia: Ambystomatidae)
journal, January 1995
- Sever, David M.; Krenz, John D.; Johnson, Kristin M.
- Journal of Morphology, Vol. 223, Issue 1
Bet-hedging as a mechanism for the evolution of polyandry, revisited: POLYANDRY AS BET-HEDGING
journal, January 2016
- Yasui, Yukio; Garcia-Gonzalez, Francisco
- Evolution, Vol. 70, Issue 2
Why do females mate multiply? A review of the genetic benefits
journal, February 2000
- Jennions, Michael D.; Petrie, Marion
- Biological Reviews, Vol. 75, Issue 1
Female sperm storage in amphibians
journal, December 2001
- Sever, David M.
- Journal of Experimental Zoology, Vol. 292, Issue 2
Genetic evidence for sexual selection in black ratsnakes, Elaphe obsoleta
journal, January 2005
- Blouin-Demers, Gabriel; Gibbs, H. Lisle; Weatherhead, Patrick J.
- Animal Behaviour, Vol. 69, Issue 1
Sexual selection
journal, February 1996
- Andersson, Malte; Iwasa, Yoh
- Trends in Ecology & Evolution, Vol. 11, Issue 2
Carolina bay wetlands: Unique habitats of the southeastern United States
journal, September 2003
- Sharitz, Rebecca R.
- Wetlands, Vol. 23, Issue 3
Remarkable Amphibian Biomass and Abundance in an Isolated Wetland: Implications for Wetland Conservation
journal, October 2006
- Gibbons, J. Whitfield; Winne, Christopher T.; Scott, David E.
- Conservation Biology, Vol. 20, Issue 5
Condition dependence of reproductive strategy and the benefits of polyandry in a viviparous lizard
journal, November 2006
- Eizaguirre, Christophe; Laloi, David; Massot, Manuel
- Proceedings of the Royal Society B: Biological Sciences, Vol. 274, Issue 1608
Spermatophores of the salamander Ambystoma texanum
journal, January 1981
- Russell, Lonnie D.; Brandon, Ronald A.; Zalisko, Edward J.
- Tissue and Cell, Vol. 13, Issue 3
The Evolution of Polyandry: Sperm Competition, Sperm Selection, and Offspring Viability
journal, December 2005
- Simmons, Leigh W.
- Annual Review of Ecology, Evolution, and Systematics, Vol. 36, Issue 1
The more the better - polyandry and genetic similarity are positively linked to reproductive success in a natural population of terrestrial salamanders (Salamandra salamandra)
journal, November 2013
- Caspers, Barbara A.; Krause, E. Tobias; Hendrix, Ralf
- Molecular Ecology, Vol. 23, Issue 1
Sexual conflict resulting from adaptations to sperm competition
journal, April 1997
- Stockley, P.
- Trends in Ecology & Evolution, Vol. 12, Issue 4
Adaptively flexible polyandry
journal, November 2013
- Gowaty, Patricia Adair
- Animal Behaviour, Vol. 86, Issue 5
Multiple paternity as genetic bet-hedging in female sierra dome spiders, Linyphia litigiosa (Linyphiidae)
journal, February 1991
- Watson, Paul J.
- Animal Behaviour, Vol. 41, Issue 2
Multiple paternity, sperm storage, and reproductive success of female and male painted turtles ( Chrysemys picta ) in nature
journal, January 2002
- Pearse, Devon; Janzen, Fred; Avise, John
- Behavioral Ecology and Sociobiology, Vol. 51, Issue 2
Direct costs and benefits of multiple mating: Are high female mating rates due to ejaculate replenishment?
journal, March 2016
- Worthington, Amy M.; Kelly, Clint D.
- Behavioural Processes, Vol. 124
A test of the genetic compatibility hypothesis with tree swallows, Tachycineta bicolor
journal, July 2005
- Barber, Colleen A.; Edwards, Mandy J.; Robertson, Raleigh J.
- Canadian Journal of Zoology, Vol. 83, Issue 7
Temporal patterns in reproduction may explain variationin mating frequencies in the green-veined white butterfly Pieris napi
journal, August 2006
- Välimäki, Panu; Kaitala, Arja; Kokko, Hanna
- Behavioral Ecology and Sociobiology, Vol. 61, Issue 1
Multiple mating increases female fitness in Drosophila simulans
journal, September 2008
- Taylor, Michelle L.; Wigmore, Clare; Hodgson, David J.
- Animal Behaviour, Vol. 76, Issue 3
Why do female Gunnison's prairie dogs copulate with more than one male?
journal, February 1998
- Hoogland, John L.
- Animal Behaviour, Vol. 55, Issue 2
True polyandry and pseudopolyandry: why does a monandrous fly remate?
journal, January 2013
- Fisher, David N.; Doff, Rowan J.; Price, Tom A. R.
- BMC Evolutionary Biology, Vol. 13, Issue 1
Polyandry is context dependent but not convenient in a mostly monandrous wasp
journal, February 2016
- Boulton, Rebecca A.; Shuker, David M.
- Animal Behaviour, Vol. 112
Multiple Mating Increases Fecundity, Fertility and Relative Clutch Mass in the Female Leopard Gecko (Eublepharis macularius)
journal, May 2008
- LaDage, Lara D.; Gutzke, William H. N.; Simmons, Richard A.
- Ethology, Vol. 114, Issue 5
Estimating Fitness: A Comparison of Body Condition Indices
journal, October 1996
- Jakob, Elizabeth M.; Marshall, Samuel D.; Uetz, George W.
- Oikos, Vol. 77, Issue 1
Post-mating sexual selection increases lifetime fitness of polyandrous females in the wild
journal, November 2006
- Fisher, Diana O.; Double, Michael C.; Blomberg, Simon P.
- Nature, Vol. 444, Issue 7115
She gets many and she chooses the best: polygynandry in Salamandrina perspicillata (Amphibia: Salamandridae)
journal, July 2015
- Rovelli, Valentina; Randi, Ettore; Davoli, Francesca
- Biological Journal of the Linnean Society, Vol. 116, Issue 3
Bet hedging via multiple mating: A meta-analysis: BET HEDGING AND MULTIPLE MATING
journal, December 2015
- Holman, Luke
- Evolution, Vol. 70, Issue 1
Statistical confidence for likelihood‐based paternity inference in natural populations
journal, May 1998
- Marshall, T. C.; Slate, J.; Kruuk, L. E. B.
- Molecular Ecology, Vol. 7, Issue 5
Variation in polyandry and its fitness consequences among populations of the red flour beetle, Tribolium castaneum
journal, January 2007
- Pai, Aditi; Feil, Stacy; Yan, Guiyun
- Evolutionary Ecology, Vol. 21, Issue 5
Isolation and characterization of microsatellite DNA loci from Ambystoma salamanders
journal, May 2005
- Croshaw, Dean A.; Schable, Nancy A.; Peters, Maureen B.
- Conservation Genetics, Vol. 6, Issue 3
Remating in Drosophila Melanogaster: are Indirect Benefits Condition Dependent?
journal, September 2010
- Long, Tristan A. F.; Pischedda, Alison; Rice, William R.
- Evolution, Vol. 64, Issue 9
Genetic and potential non-genetic benefits increase offspring fitness of polyandrous females in non-resource based mating system
journal, January 2010
- Kekäläinen, Jukka; Rudolfsen, Geir; Janhunen, Matti
- BMC Evolutionary Biology, Vol. 10, Issue 1
Comparing the performance of analytical techniques for genetic parentage of half-sib progeny arrays
journal, October 2009
- Croshaw, Dean A.; Peters, Maureen B.; Glenn, Travis C.
- Genetics Research, Vol. 91, Issue 5
The Effect of Larval Density on Adult Demographic Traits in Ambystoma Opacum
journal, July 1994
- Scott, David E.
- Ecology, Vol. 75, Issue 5
Intra-sexual selection in Drosophila
journal, December 1948
- Bateman, A. J.
- Heredity, Vol. 2, Issue 3
Effects of Larval Density in Ambystoma Opacum: An Experiment Large-Scale Field Enclosures
journal, February 1990
- Scott, David E.
- Ecology, Vol. 71, Issue 1
Effects of simultaneous polyandry on offspring fitness in an African tree frog
journal, January 2011
- Byrne, Phillip G.; Whiting, Martin J.
- Behavioral Ecology, Vol. 22, Issue 2
Fallow deer polyandry is related to fertilization insurance
journal, January 2013
- Briefer, Elodie F.; Farrell, Mary E.; Hayden, Thomas J.
- Behavioral Ecology and Sociobiology, Vol. 67, Issue 4
Relatedness, body size and paternity in the alpine newt, Triturus alpestris
journal, March 2003
- Garner, Trenton W. J.; Schmidt, Benedikt R.
- Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 270, Issue 1515
Multiple insemination increases reproductive success of female Montandon's newt ( Triturus montandoni , Caudata, Salamandridae)
journal, January 2001
- Osikowski, Artur; Rafin´ski, Jan
- Behavioral Ecology and Sociobiology, Vol. 49, Issue 2-3
Why do female adders copulate so frequently?
journal, January 1992
- Madsen, Thomas; Shine, Richard; Loman, Jon
- Nature, Vol. 355, Issue 6359
Advantages of Multiple Matings to Females: a test of the Infertility Hypothesis Using Lizards
journal, October 1997
- Olsson, Mats; Shine, Richard
- Evolution, Vol. 51, Issue 5
The evolution of polyandry: multiple mating and female fitness in insects
journal, August 2000
- Arnqvist, Göran; Nilsson, Tina
- Animal Behaviour, Vol. 60, Issue 2
Polyandry in grain beetles, Tenebrio molitor, leads to greater reproductive success: material or genetic benefits?
journal, November 2001
- Worden, B. D.
- Behavioral Ecology, Vol. 12, Issue 6
A "Good-Sperm" Model Can Explain the Evolution of Costly Multiple Mating by Females
journal, March 1997
- Yasui, Yukio
- The American Naturalist, Vol. 149, Issue 3
Female multiple mating for fertility assurance in red flour beetles ( Tribolium castaneum )
journal, July 2005
- Pai, Aditi; Bennett, Lauren; Yan, Guiyun
- Canadian Journal of Zoology, Vol. 83, Issue 7
Polyandry Promotes Enhanced Offspring Survival in Decorated Crickets
journal, January 2005
- Ivy, Tracie M.; Sakaluk, Scott K.
- Evolution, Vol. 59, Issue 1
Multiple mating by females is not dependent on body size in the salamander Desmognathus ochrophaeus
journal, January 1996
- Shillington, Cara; Verrell, Paul
- Amphibia-Reptilia, Vol. 17, Issue 1
Fitness benefits of polyandry for experienced females: BREEDING EXPERIENCE AND POLYANDRY
journal, April 2010
- Whittingham, L. A.; Dunn, P. O.
- Molecular Ecology, Vol. 19, Issue 11
Quantifying sexual selection: a comparison of competing indices with mating system data from a terrestrially breeding salamander: INDICES FOR MEASURING SEXUAL SELECTION
journal, December 2009
- Croshaw, Dean A.
- Biological Journal of the Linnean Society, Vol. 99, Issue 1