Close‐kin mating, but not inbred parents, reduces hatching rates and offspring quality in a threatened tortoise

Yuan, Michael L.; White, K. Nicole; Rothermel, Betsie B.; Zamudio, Kelly R.; Tuberville, Tracey D.

doi:10.1111/jeb.13518

Title: Close‐kin mating, but not inbred parents, reduces hatching rates and offspring quality in a threatened tortoise

Journal Article · 02 September 2019 · Journal of Evolutionary Biology

DOI: https://doi.org/10.1111/jeb.13518 · OSTI ID:1560261

^[1];

^[2]; Rothermel, Betsie B. ^[3];

^[4]; Tuberville, Tracey D. ^[5]

Department of Environmental Science, Policy, and Management College of Natural Resources University of California Berkeley CA USA, Archbold Biological Station Venus FL USA
Archbold Biological Station Venus FL USA, Savannah River Ecology Laboratory University of Georgia Aiken SC USA, Daniel B. Warnell School of Forestry and Natural Resources University of Georgia Athens GA USA
Archbold Biological Station Venus FL USA
Department of Ecology and Evolutionary Biology Cornell University Ithaca NY USA
Savannah River Ecology Laboratory University of Georgia Aiken SC USA

Abstract Inbreeding depression, the reduction in fitness due to mating of related individuals, is of particular conservation concern in species with small, isolated populations. Although inbreeding depression is widespread in natural populations, long‐lived species may be buffered from its effects during population declines due to long generation times and thus are less likely to have evolved mechanisms of inbreeding avoidance than species with shorter generation times. However, empirical evidence of the consequences of inbreeding in threatened, long‐lived species is limited. In this study, we leverage a well‐studied population of gopher tortoises, Gopherus polyphemus , to examine the role of inbreeding depression and the potential for behavioural inbreeding avoidance in a natural population of a long‐lived species. We tested the hypothesis that increased parental inbreeding leads to reduced hatching rates and offspring quality. Additionally, we tested for evidence of inbreeding avoidance. We found that high parental relatedness results in offspring with lower quality and that high parental relatedness is correlated with reduced hatching success. However, we found that hatching success and offspring quality increase with maternal inbreeding, likely due to highly inbred females mating with more distantly related males. We did not find evidence for inbreeding avoidance in males and outbred females, suggesting sex‐specific evolutionary trade‐offs may have driven the evolution of mating behaviour. Our results demonstrate inbreeding depression in a long‐lived species and that the evolution of inbreeding avoidance is shaped by multiple selective forces.

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Sponsoring Organization:: USDOE

Grant/Contract Number:: EM0004391

OSTI ID:: 1560261

Journal Information:: Journal of Evolutionary Biology, Journal Name: Journal of Evolutionary Biology Journal Issue: 10 Vol. 32; ISSN 1010-061X

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: Country unknown/Code not available

Language:: English

References (86)

Effects of predator exclusion on nest and hatchling survival in the gopher tortoise Smith, Lora L.; Steen, David A.; Conner, L. Mike The Journal of Wildlife Management, Vol. 77, Issue 2 https://doi.org/10.1002/jwmg.449	journal	August 2012
Mate choice in the face of both inbreeding and outbreeding depression in the intertidal copepod Tigriopus californicus Palmer, C. A.; Edmands, S. Marine Biology, Vol. 136, Issue 4 https://doi.org/10.1007/s002270050729	journal	May 2000
Isolation and characterization of polymorphic microsatellite loci for the gopher tortoise (Gopherus polyphemus) and cross-amplification in other species of Gopherus Kreiser, Brian R.; Ennen, Joshua R.; Gaillard, Daniel L. Conservation Genetics Resources, Vol. 5, Issue 1 https://doi.org/10.1007/s12686-012-9781-8	journal	October 2012
Sex-biased dispersal and inbreeding avoidance in birds and mammals Pusey, Anne E. Trends in Ecology & Evolution, Vol. 2, Issue 10 https://doi.org/10.1016/0169-5347(87)90081-4	journal	October 1987
Inbreeding avoidance in animals Pusey, Anne; Wolf, Marisa Trends in Ecology & Evolution, Vol. 11, Issue 5 https://doi.org/10.1016/0169-5347(96)10028-8	journal	May 1996
Regression-based tests for overdispersion in the Poisson model Cameron, A. Colin; Trivedi, Pravin K. Journal of Econometrics, Vol. 46, Issue 3 https://doi.org/10.1016/0304-4076(90)90014-K	journal	December 1990
Considering evolutionary processes in conservation biology Crandall, Keith A.; Bininda-Emonds, Olaf R. P.; Mace, Georgina M. Trends in Ecology & Evolution, Vol. 15, Issue 7 https://doi.org/10.1016/S0169-5347(00)01876-0	journal	July 2000
Inbreeding effects in wild populations Keller, L. Trends in Ecology & Evolution, Vol. 17, Issue 5 https://doi.org/10.1016/S0169-5347(02)02489-8	journal	May 2002
Hatch size, somatic growth rate and size-dependent survival in the endangered ploughshare tortoise O’Brien, Susan; Robert, Bourou; Tiandray, Hafany Biological Conservation, Vol. 126, Issue 2 https://doi.org/10.1016/j.biocon.2005.03.022	journal	November 2005
Declines of the gopher tortoise on protected lands McCoy, Earl D.; Mushinsky, Henry R.; Lindzey, Jonathan Biological Conservation, Vol. 128, Issue 1 https://doi.org/10.1016/j.biocon.2005.09.021	journal	February 2006
Realistic levels of inbreeding depression strongly affect extinction risk in wild populations O’Grady, Julian J.; Brook, Barry W.; Reed, David H. Biological Conservation, Vol. 133, Issue 1 https://doi.org/10.1016/j.biocon.2006.05.016	journal	November 2006
Long-term apparent survival of translocated gopher tortoises: A comparison of newly released and previously established animals Tuberville, Tracey D.; Norton, Terry M.; Todd, Brian D. Biological Conservation, Vol. 141, Issue 11 https://doi.org/10.1016/j.biocon.2008.08.004	journal	November 2008
Mating system in a gopher tortoise population established through multiple translocations: Apparent advantage of prior residence Tuberville, Tracey D.; Norton, Terry M.; Waffa, Bradley J. Biological Conservation, Vol. 144, Issue 1 https://doi.org/10.1016/j.biocon.2010.08.012	journal	January 2011
No paternal genetic integration in desert tortoises (Gopherus agassizii) following translocation into an existing population Mulder, Kevin P.; Walde, Andrew D.; Boarman, William I. Biological Conservation, Vol. 210 https://doi.org/10.1016/j.biocon.2017.04.030	journal	June 2017
Genetic rescue to the rescue Whiteley, Andrew R.; Fitzpatrick, Sarah W.; Funk, W. Chris Trends in Ecology & Evolution, Vol. 30, Issue 1 https://doi.org/10.1016/j.tree.2014.10.009	journal	January 2015
Estimators for pairwise relatedness and individual inbreeding coefficients Ritland, Kermit Genetical Research, Vol. 67, Issue 2 https://doi.org/10.1017/S0016672300033620	journal	April 1996
Inbreeding depression due to mildly deleterious mutations in finite populations: size does matter Bataillon, Thomas; Kirkpatrick, Mark Genetical Research, Vol. 75, Issue 1 https://doi.org/10.1017/S0016672399004048	journal	February 2000
Genetic Effects of a Persistent Bottleneck on a Natural Population of Ornate Box Turtles (Terrapene ornata) Kuo, Chih-Horng; Janzen, Fredric J. Conservation Genetics, Vol. 5, Issue 4 https://doi.org/10.1023/B:COGE.0000041020.54140.45	journal	August 2004
Intra-sexual selection in Drosophila Bateman, A. J. Heredity, Vol. 2, Issue 3 https://doi.org/10.1038/hdy.1948.21	journal	December 1948
Purging inbreeding depression and the probability of extinction: full-sib mating Hedrick, Philip W. Heredity, Vol. 73, Issue 4 https://doi.org/10.1038/hdy.1994.183	journal	October 1994
Inbreeding in the wild really does matter Frankham, R. Heredity, Vol. 104, Issue 2 https://doi.org/10.1038/hdy.2009.155	journal	November 2009
Inbreeding depression in benign and stressful environments Armbruster, P.; Reed, D. H. Heredity, Vol. 95, Issue 3 https://doi.org/10.1038/sj.hdy.6800721	journal	August 2005
When does conservation genetics matter? Amos, William; Balmford, Andrew Heredity, Vol. 87, Issue 3 https://doi.org/10.1046/j.1365-2540.2001.00940.x	journal	September 2001
Experimental analysis of an early life-history stage: avian predation selects for larger body size of hatchling turtles Janzen, F. J.; Tucker, J. K.; Paukstis, G. L. Journal of Evolutionary Biology, Vol. 13, Issue 6 https://doi.org/10.1046/j.1420-9101.2000.00234.x	journal	November 2000
Microsatellite loci for the North American tortoises (genus Gopherus) and their applicability to other turtle species Schwartz, T. S.; Osentoski, M.; Lamb, T. Molecular Ecology Notes, Vol. 3, Issue 2 https://doi.org/10.1046/j.1471-8286.2003.00428.x	journal	June 2003
Inbreeding and Extinction: A Threshold Effect Frankham, Richard Conservation Biology, Vol. 9, Issue 4 https://doi.org/10.1046/j.1523-1739.1995.09040792.x	journal	August 1995
The frequency distribution of lethal chromosomes in finite populations. Nei, M. Proceedings of the National Academy of Sciences, Vol. 60, Issue 2 https://doi.org/10.1073/pnas.60.2.517	journal	June 1968
Genetic benefits enhance the reproductive success of polyandrous females Newcomer, S. D.; Zeh, J. A.; Zeh, D. W. Proceedings of the National Academy of Sciences, Vol. 96, Issue 18 https://doi.org/10.1073/pnas.96.18.10236	journal	August 1999
When Should Animals Tolerate Inbreeding? Waser, Peter M.; Austad, Steven N.; Keane, Brian The American Naturalist, Vol. 128, Issue 4 https://doi.org/10.1086/284585	journal	October 1986
Mutation Accumulation and the Extinction of Small Populations Lynch, Michael; Conery, John; Burger, Reinhard The American Naturalist, Vol. 146, Issue 4 https://doi.org/10.1086/285812	journal	October 1995
Local Competition, Inbreeding, and the Evolution of Sex‐Biased Dispersal Perrin, Nicolas; Mazalov, Vladimir The American Naturalist, Vol. 155, Issue 1 https://doi.org/10.1086/303296	journal	January 2000
The Effects of a Bottleneck on Inbreeding Depression and the Genetic Load Kirkpatrick, Mark; Jarne, Philippe The American Naturalist, Vol. 155, Issue 2 https://doi.org/10.1086/303312	journal	February 2000
Inbreeding Avoidance through Kin Recognition: Choosy Females Boost Male Dispersal Lehmann, Laurent; Perrin, Nicolas The American Naturalist, Vol. 162, Issue 5 https://doi.org/10.1086/378823	journal	November 2003
No evidence of inbreeding avoidance or inbreeding depression in a social carnivore Keane, Brian; Creel, Scott R.; Waser, Peter M. Behavioral Ecology, Vol. 7, Issue 4 https://doi.org/10.1093/beheco/7.4.480	journal	January 1996
A theory of mate choice based on heterozygosity Brown, Jerram L. Behavioral Ecology, Vol. 8, Issue 1 https://doi.org/10.1093/beheco/8.1.60	journal	January 1997
An Estimator for Pairwise Relatedness Using Molecular Markers Wang, Jinliang Genetics, Vol. 160, Issue 3 https://doi.org/10.1093/genetics/160.3.1203	journal	March 2002
Patterns of Inbreeding Depression and Architecture of the Load in Subdivided Populations Glémin, Sylvain; Ronfort, Joëlle; Bataillon, Thomas Genetics, Vol. 165, Issue 4 https://doi.org/10.1093/genetics/165.4.2193	journal	December 2003
Multiple Paternity and Breeding System in the Gopher Tortoise, Gopherus polyphemus Moon, Jamie C.; McCoy, Earl D.; Mushinsky, Henry R. Journal of Heredity, Vol. 97, Issue 2 https://doi.org/10.1093/jhered/esj017	journal	February 2006
Inbreeding depression influences lifetime breeding success in a wild population of red deer ( Cervus elaphus ) Slate, J.; Kruuk, L. E. B.; Marshall, T. C. Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 267, Issue 1453 https://doi.org/10.1098/rspb.2000.1192	journal	August 2000
Sex–specific, counteracting responses to inbreeding in a bird Pizzari, T.; Lø, H.; Cornwallis, C. K. Proceedings of the Royal Society of London. Series B: Biological Sciences, Vol. 271, Issue 1553 https://doi.org/10.1098/rspb.2004.2843	journal	October 2004
A new theory for the evolution of polyandry as a means of inbreeding avoidance Cornell, Stephen J.; Tregenza, Tom Proceedings of the Royal Society B: Biological Sciences, Vol. 274, Issue 1627 https://doi.org/10.1098/rspb.2007.0926	journal	September 2007
Genetic load, inbreeding depression, and hybrid vigor covary with population size: An empirical evaluation of theoretical predictions: GENETIC LOAD AND POPULATION SIZE IN Lohr, Jennifer N.; Haag, Christoph R. Evolution, Vol. 69, Issue 12 https://doi.org/10.1111/evo.12802	journal	November 2015
Lethals in Finite Populations Hedrick, Philip W. Evolution, Vol. 56, Issue 3 https://doi.org/10.1111/j.0014-3820.2002.tb01374.x	journal	March 2002
Environmental Conditions Affect the Magnitude of Inbreeding Depression in Survival of Darwin'S Finches Keller, Lukas F.; Grant, Peter R.; Grant, B. Rosemary Evolution, Vol. 56, Issue 6 https://doi.org/10.1111/j.0014-3820.2002.tb01434.x	journal	June 2002
Field use of Maximal Sprint Speed by Collared Lizards (Crotaphytus Collaris): Compensation and Sexual Selection Husak, Jerry F.; Fox, Stanley F. Evolution, Vol. 60, Issue 9 https://doi.org/10.1111/j.0014-3820.2006.tb00532.x	journal	September 2006
When not to Avoid Inbreeding Kokko, Hanna; Ots, Indrek Evolution, Vol. 60, Issue 3 https://doi.org/10.1111/j.0014-3820.2006.tb01128.x	journal	March 2006
Longterm effects of incubation temperatures on the morphology and locomotor performance of hatchling lizards (Bassiana duperreyi, Scincidae) Elphick, Melanie J.; Shine, Richard Biological Journal of the Linnean Society, Vol. 63, Issue 3 https://doi.org/10.1111/j.1095-8312.1998.tb01527.x	journal	March 1998
Intraspecific phylogeography of the gopher tortoise, Gopherus polyphemus: RFLP analysis of amplified mtDNA segments Osentoski, M. F.; Lamb, T. Molecular Ecology, Vol. 4, Issue 6 https://doi.org/10.1111/j.1365-294X.1995.tb00271.x	journal	December 1995
High genetic diversity and no inbreeding in the endangered copper redhorse, Moxostoma hubbsi (Catostomidae, Pisces): the positive sides of a long generation time: CONSERVATION GENETICS OF THE COPPER REDHORSE LippÉ, Catherine; Dumont, Pierre; Bernatchez, Louis Molecular Ecology, Vol. 15, Issue 7 https://doi.org/10.1111/j.1365-294X.2006.02902.x	journal	March 2006
Revising how the computer program cervus accommodates genotyping error increases success in paternity assignment: CERVUS LIKELIHOOD MODEL Kalinowski, Steven T.; Taper, Mark L.; Marshall, Tristan C. Molecular Ecology, Vol. 16, Issue 5 https://doi.org/10.1111/j.1365-294X.2007.03089.x	journal	February 2007
Reliable selfing rate estimates from imperfect population genetic data David, Patrice; Pujol, BenoÎT; Viard, FrÉDÉRique Molecular Ecology, Vol. 16, Issue 12 https://doi.org/10.1111/j.1365-294X.2007.03330.x	journal	June 2007
Behavioural inbreeding avoidance in wild African elephants: ELEPHANTS AVOID INBREEDING Archie, Elizabeth A.; Hollister-Smith, Julie A.; Poole, Joyce H. Molecular Ecology, Vol. 16, Issue 19 https://doi.org/10.1111/j.1365-294X.2007.03483.x	journal	September 2007
Identifying Populations for Conservation on the Basis of Genetic Markers Petit, Rémy J.; El Mousadik, Abdelhamid; Pons, Odile Conservation Biology, Vol. 12, Issue 4 https://doi.org/10.1111/j.1523-1739.1998.96489.x	journal	August 1998
A COMPARATIVE ANALYSIS OF THE ECOLOGICAL SIGNIFICANCE OF MAXIMAL LOCOMOTOR PERFORMANCE IN CARIBBEAN ANOLIS LIZARDS Irschick, Duncan J.; Losos, Jonathan B. Evolution, Vol. 52, Issue 1 https://doi.org/10.1111/j.1558-5646.1998.tb05155.x	journal	February 1998
A Comparison of Inbreeding Depression in Life-History and Morphological Traits in Animals DeRose, Marc A.; Roff, Derek A. Evolution, Vol. 53, Issue 4 https://doi.org/10.1111/j.1558-5646.1999.tb04541.x	journal	August 1999
Heterozygosity-Fitness Correlations: a time for Reappraisal Szulkin, Marta; Bierne, Nicolas; David, Patrice Evolution https://doi.org/10.1111/j.1558-5646.2010.00966.x	journal	March 2010
COLONY: a program for parentage and sibship inference from multilocus genotype data Jones, Owen R.; Wang, Jinliang Molecular Ecology Resources, Vol. 10, Issue 3 https://doi.org/10.1111/j.1755-0998.2009.02787.x	journal	May 2010
coancestry: a program for simulating, estimating and analysing relatedness and inbreeding coefficients: COMPUTER PROGRAM NOTE Wang, Jinliang Molecular Ecology Resources, Vol. 11, Issue 1 https://doi.org/10.1111/j.1755-0998.2010.02885.x	journal	December 2010
Outbreeding avoidance as probable driver of mate choice in the Asiatic toad: Outbreeding avoidance of Asiatic toads Luo, Z.; Hu, M.; Hong, M. Journal of Zoology, Vol. 295, Issue 3 https://doi.org/10.1111/jzo.12183	journal	November 2014
Consequences of maternal effects on offspring size, growth and survival in the desert tortoise: Maternal body size and offspring fitness Nafus, M. G.; Todd, B. D.; Buhlmann, K. A. Journal of Zoology, Vol. 297, Issue 2 https://doi.org/10.1111/jzo.12250	journal	April 2015
Kinship, inbreeding and fine-scale spatial structure influence gut microbiota in a hindgut-fermenting tortoise Yuan, Michael L.; Dean, Samantha H.; Longo, Ana V. Molecular Ecology, Vol. 24, Issue 10 https://doi.org/10.1111/mec.13169	journal	April 2015
Cryptic inbreeding depression in a growing population of a long-lived species Taylor, Helen R.; Colbourne, Rogan M.; Robertson, Hugh A. Molecular Ecology, Vol. 26, Issue 3 https://doi.org/10.1111/mec.13977	journal	January 2017
An experimental study of inbreeding depression in a natural habitat Jimenez, J.; Hughes, K.; Alaks, G. Science, Vol. 266, Issue 5183 https://doi.org/10.1126/science.7939661	journal	October 1994
The effects of constant and fluctuating incubation temperatures on sex determination, growth, and performance in the tortoise Gopherus polyphemus Demuth, Jeffery P. Canadian Journal of Zoology, Vol. 79, Issue 9 https://doi.org/10.1139/cjz-79-9-1609	journal	January 2001
Sexual size dimorphism in steppe tortoises ( Testudo horsfieldi ): growth, maturity, and individual variation Lagarde, Frédéric; Bonnet, Xavier; Henen, Brian T. Canadian Journal of Zoology, Vol. 79, Issue 8 https://doi.org/10.1139/z01-097	journal	August 2001
Inbreeding Depression and its Evolutionary Consequences Charlesworth, D.; Charlesworth, B. Annual Review of Ecology and Systematics, Vol. 18, Issue 1 https://doi.org/10.1146/annurev.es.18.110187.001321	journal	November 1987
The Cost of Sex: Quantifying Energetic Investment in Gamete Production by Males and Females Hayward, April; Gillooly, James F. PLoS ONE, Vol. 6, Issue 1 https://doi.org/10.1371/journal.pone.0016557	journal	January 2011
Turtle Carapace Anomalies: The Roles of Genetic Diversity and Environment Velo-Antón, Guillermo; Becker, C. Guilherme; Cordero-Rivera, Adolfo PLoS ONE, Vol. 6, Issue 4 https://doi.org/10.1371/journal.pone.0018714	journal	April 2011
Understanding and Predicting the Fitness Decline of Shrunk Populations: Inbreeding, Purging, Mutation, and Standard Selection García-Dorado, Aurora Genetics, Vol. 190, Issue 4 https://doi.org/10.1534/genetics.111.135541	journal	January 2012
Geographic Variation in Body and Clutch Size of Gopher Tortoises Ashton, Kyle G.; Burke, Russell L.; Layne, James N. Copeia, Vol. 2007, Issue 2 https://doi.org/10.1643/0045-8511(2007)7[355:GVIBAC]2.0.CO;2	journal	May 2007
Mating Opportunities of Female Gopher Tortoises, Gopherus polyphemus, in Relation to Spatial Isolation of Females and Their Burrows Boglioli, Melissa D.; Guyer, Craig; Michener, William K. Copeia, Vol. 2003, Issue 4 https://doi.org/10.1643/h202-009.1	journal	December 2003
Patterns of Dispersion and Burrow Use Support Scramble Competition Polygyny in Gopherus polyphemus Johnson, Valerie M.; Guyer, Craig; Hermann, Sharon M. Herpetologica, Vol. 65, Issue 2 https://doi.org/10.1655/08-029R.1	journal	June 2009
Low Genetic Diversity in Several Gopher Tortoise (Gopherus polyphemus) Populations in the Desoto National Forest, Mississippi Ennen, Joshua R.; Kreiser, Brian R.; Qualls, Carl P. Herpetologica, Vol. 66, Issue 1 https://doi.org/10.1655/08-083.1	journal	March 2010
A Comparison of Artificial Incubation and Natural Incubation Hatching Success of Gopher Tortoise ( Gopherus polyphemus ) Eggs In Southern Mississippi Noel, Krista M.; Qualls, Carl P.; Ennen, Joshua R. Herpetologica, Vol. 68, Issue 3 https://doi.org/10.1655/HERPETOLOGICA-D-11-00061.1	journal	September 2012
Effects of Population Density On Patterns of Movement and Behavior of Gopher Tortoises (Gopherus polyphemus) Guyer, Craig; Johnson, Valerie M.; Hermann, Sharon M. Herpetological Monographs, Vol. 26, Issue 1 https://doi.org/10.1655/HERPMONOGRAPHS-D-10-00004.1	journal	December 2012
Factors Influencing Reproductive Output and Egg Size in a Southern Population of Gopher Tortoises Rothermel, Betsie B.; Castellón, Traci D. Southeastern Naturalist, Vol. 13, Issue 4 https://doi.org/10.1656/058.013.0403	journal	December 2014
Nesting and Hatchling Ecology of Gopher Tortoises (Gopherus polyphemus) in Southern Mississippi Epperson, Deborah M.; Heise, Colleen D. Journal of Herpetology, Vol. 37, Issue 2 https://doi.org/10.1670/0022-1511(2003)037[0315:NAHEOG]2.0.CO;2	journal	April 2003
Gopher Tortoise (Gopherus polyphemus) Abundance and Distribution after Prescribed Fire Reintroduction to Florida Scrub and Sandhill at Archbold Biological Station Ashton, Kyle G.; Engelhardt, Blake M.; Branciforte, Brian S. Journal of Herpetology, Vol. 42, Issue 3 https://doi.org/10.1670/06-246.1	journal	September 2008
Rapid development of gene-tagged microsatellite markers from bacterial artificial chromosome clones using anchored TAA repeat primers Waldbieser, Geoffrey C.; Quiniou, Sylvie M. A.; Karsi, Attila BioTechniques, Vol. 35, Issue 5 https://doi.org/10.2144/03355st05	journal	November 2003
Studies on the Chemistry and Social Significance of Chin Gland Secretions in the Desert Tortoise, Gopherus agassizii Alberts, Allison C.; Rostal, David C.; Lance, Valentine A. Herpetological Monographs, Vol. 8 https://doi.org/10.2307/1467075	journal	January 1994
Population Structure of Gopherus polyphemus in Northern Florida Alford, Ross A. Journal of Herpetology, Vol. 14, Issue 2 https://doi.org/10.2307/1563851	journal	June 1980
Survivorship and Predation of Hatchling and Yearling Gopher Tortoises, Gopherus polyphemus Butler, Joseph A.; Sowell, Scott Journal of Herpetology, Vol. 30, Issue 3 https://doi.org/10.2307/1565195	journal	September 1996
An Experimental Analysis of Natural Selection on Body Size of Hatchling Turtles Janzen, Fredric J. Ecology, Vol. 74, Issue 2 https://doi.org/10.2307/1939296	journal	March 1993
Range-Wide and Regional Patterns of Population Structure and Genetic Diversity in the Gopher Tortoise Gaillard, D.; Ennen, J. R.; Kreiser, B. R. Journal of Fish and Wildlife Management, Vol. 8, Issue 2 https://doi.org/10.3996/022017-JFWM-010	journal	December 2017
Mitochondrial DNA Assessment of the Phylogeography of the Gopher Tortoise Ennen, Joshua R.; Kreiser, Brian R.; Qualls, Carl P. Journal of Fish and Wildlife Management, Vol. 3, Issue 1 https://doi.org/10.3996/102011-JFWM-063	journal	June 2012
Angiographic, Anatomic and Clinical Technique Descriptions of A Subcarapacial Venipuncture Site for Chelonians Hernandez-Divers, Sonia M.; Hernandez-Divers, Stephen J.; Wyneken, Jeanette Journal of Herpetological Medicine and Surgery, Vol. 12, Issue 2 https://doi.org/10.5818/1529-9651.12.2.32	journal	January 2002

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