Abstract
Conservation breeding programs have long been an important management tool for species recovery. Recently, breeding programs have begun to integrate next generation sequencing data into pedigree-based management strategies designed to maximize retention of genetic diversity and minimize inbreeding. In 2005, an ex situ breeding program for two of the three extant, geographically separate populations of the endangered southern mountain yellow-legged frog (Rana muscosa) was established at the San Diego Zoo Wildlife Alliance. To provide improved breeding recommendations for the species, we conducted molecular population genetic assessments using double digest restriction site-associated DNA sequencing data. We first studied genetic diversity, population differentiation, and genetic structure of wild frogs to validate the status of management units in R. muscosa. Genetic diversity was relatively low (HO = 0.166–0.245), population differentiation moderate (FST = 0.29), and patterns of genetic structure and admixture supported the evolutionary divergence of frogs by mountain ranges with limited gene flow. In the breeding program, relatedness estimates identified close relatives amongst the founders, and molecularly-derived kinship values were used to determine and rank suitable breeders to minimize population mean kinship. Ex situ management recommendations highlight the need for importing additional founders from the wild to enhance genetic diversity in the breeding program, as an effective source for genetic restoration. Alternatively, the use of advanced reproductive technologies to capture wild diversity without removal of individuals from the wild seem promising.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Supplementary tables with sample and sequence read information are deposited in the Dryad data repository (https://doi.org/10.5061/dryad.5tb2rbpbb and https://doi.org/10.5061/dryad.95x69p8rq). Raw sequence reads are deposited at NCBI (Project number PRJNA1061082). Scripts for selecting Stacks parameter settings are available on GitHub (https://github.com/apwilder/StacksParameterSelection).
References
Addis BR, Lowe WH, Hossack BR, Allendorf FW (2015) Population genetic structure and disease in montane boreal toads: more heterozygous individuals are more likely to be infected with amphibian chytrid. Conserv Genet 16:833–844. https://doi.org/10.1007/s10592-015-0704-6
Allentoft M, O’Brien J (2010) Global amphibian declines loss of genetic diversity and fitness: a review. Diversity 2:47–71. https://doi.org/10.3390/d2010047
Almond REA, Grooten M, Peterson T (2022) Living planet report 2020: bending the curve of biodiversity loss. https://pure.iiasa.ac.at/id/eprint/16870/
Andrews S (2010) FastQC: a quality control yool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/
Backlin AR, Hitchcock CJ, Gallegos EA, Yee JL, Fisher RN (2013) The precarious persistence of the endangered Sierra Madre yellow-legged frog Rana muscosa in southern California, USA. Oryx 49:157–164. https://doi.org/10.1017/S003060531300029X
Backlin AR, Gallegos EA, Hitchcock CJ, Heath JN, Fisher RN (2022) Southern California Mountain Yellow-legged Frog (Rana muscosa). Data Summary, USGS, USA
Ballou JD, Lees C, Faust LJ, Long S, Lynch C, Bingaman Lackey L, Foose TJ (2010) Demographic and genetic management of captive populations. In: Kleiman DG, Thompson K, Kirk-Baer C (eds) Wild mammals in captivity. University of Chicago Press, Chicago, pp 219–252
Blaustein AR, Romansic JM, Kiesecker JM, Hatch AC (2003) Ultraviolet radiation toxic chemicals and amphibian population declines. Divers Distrib 9:123–140. https://doi.org/10.1046/j.1472-4642.2003.00015.x
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 15:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Browne RK, Silla AJ, Upton R et al (2019) Sperm collection and storage for the sustainable management of amphibian biodiversity. Theriogenology 133:187–200. https://doi.org/10.1016/j.theriogenology.2019.03.035
Burger I, Julien AR, Kouba AJ et al (2021) Linking in-situ and ex-situ populations of threatened amphibians through genome banking. Conserv Sci Pract 3:e525. https://doi.org/10.1111/csp2.525
Butchart S, Walpole M, Collen B et al (2010) Global biodiversity: indicators of recent declines. Science 328:1164–1168. https://doi.org/10.1126/science.118751
Byrne PG, Silla AJ (2020) An experimental test of the genetic consequences of population augmentation in an amphibian. Conserv Sci Pract 2:e194. https://doi.org/10.1111/csp2.194
Byrne AQ, Rothstein AP, Smith LL et al (2023) Revisiting conservation units for the endangered mountain yellow-legged frog species complex (Rana muscosa, Rana sierra) using multiple genomic methods
Carey C, Alexander MA (2003) Climate change and amphibian declines: is there a link? Divers Distrib 9:111–121. https://doi.org/10.1046/j.1472-4642.2003.00011.x
Carrillo L, Johnson K, Mendelson JR III (2015) Principles of program development and management for amphibian conservation captive breeding programs. Int Zoo News 62:96–107
Catchen JM, Amores A, Hohenlohe P, Cresko W, Postlethwait JH (2011) Stacks: building and genotyping Loci de novo from short-read sequences. G3 1:171–82. https://doi.org/10.1534/g3.111.000240
Coates DJ, Byrne M, Moritz C (2018) Genetic diversity and conservation units: dealing with the species-population continuum in the age of genomics. Front Ecol Evol. https://doi.org/10.3389/fevo.2018.00165
Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST, McVean G, Durbin R (2011) 1000 genomes project analysis group. The variant call format and VCFtools. Bioinformatics 27:2156–2158. https://doi.org/10.1093/bioinformatics/btr330
Darrel FR (2021) Rana muscosa Camp, 1917. Amphibian species of the world: an online reference. version 6.1. American Museum of Natural History. doi:https://doi.org/10.5531/db.vz.0001.
Daszak P, Cunningham AA, Hyatt AD (2003) Infectious disease and amphibian population declines. Divers Distrib 9:141–150. https://doi.org/10.1046/j.1472-4642.2003.00016.x
Davidson C, Shaffer HB, Jennings MR (2001) Declines of the California red-legged frog: climate UV-B habitat and pesticides hypotheses. Ecol Appl 11:464–479. https://doi.org/10.2307/3060902
Della Togna G, Howell LG, Clulow J, Langhorne CJ, Marcec-Greaves R, Calatayud NE (2020) Evaluating amphibian biobanking and reproduction for captive breeding programs according to the Amphibian Conservation Action Plan objectives. Theriogenology 150:412–431. https://doi.org/10.1016/j.theriogenology.2020.02.024
Dou J, Sun B, Sim X et al (2017) Estimation of kinship coefficient in structured and admixed populations using sparse sequencing data. PLoS Genet 13:e1007021. https://doi.org/10.1371/journal.pgen.1007021
Earl DA, vonHoldt BM (2012) Structure Harvester: a website and program for visualizing Structure output and implementing the Evanno method. Conserv Genet Resour 4:359–361. https://doi.org/10.1007/s12686-011-9548-7
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Faust LJ, Bergstrom YM, Thompson SD, Bier L (2019) PopLink version 25. Lincoln Park Zoo, Chicago
Fisher RN (2020) Southern California mountain yellow-legged frog (Rana muscosa). Data Summary, USGS, USA
Fisher RN, Shaffer HB (1996) The decline of amphibians in California’s Great Central Valley. Conser Biol 10:1387–1397
Fitzpatrick SW, Bradburd GS, Kremer CT, Salerno PE, Angeloni LM, Funk WC (2020) Genomic and fitness consequences of genetic rescue in wild populations. Curr Biol 30:517-522e5. https://doi.org/10.1016/j.cub.2019.11.062
Forzán MJ, Vanderstichel RV, Ogbuah CT, Barta JR, Smith TG (2012) Blood collection from the facial (maxillary)/musculo-cutaneous vein in true frogs (Family Ranidae). J Wildlife Dis 48:176–180. https://doi.org/10.7589/0090-3558-48.1.176
Frankham R (2015) Genetic rescue of small inbred populations: meta-analysis reveals large and consistent benefits of gene flow. Mol Ecol 24:2610–2618. https://doi.org/10.1111/mec.13139
Frankham R, Ballou JD, Briscoe DA (2010) Introduction to conservation genetics, 2nd edn. Cambridge University Press, UK
Fredrickson RJ, Siminski P, Woolf M, Hedrick PW (2007) Genetic rescue and inbreeding depression in Mexican wolves. Proc Biol Sci B 274:2365–2371. https://doi.org/10.1098/rspb.2007.0785
Funk WC, Zamudio KR, Crawford AJ (2018) Advancing understanding of amphibian evolution, ecology, behavior, and conservation with massively parallel sequencing. In: Hohenlohe PA, Rajora OP (eds) Population genomics: wildlife. Population genomics. Springer, Cham, pp 211–254. https://doi.org/10.1007/13836_2018_61
Gallegos EA, Backlin AR, Wong MN, Hitchcock CJ, Fisher RN (2020) Southern California mountain yellow-legged frog (Rana muscosa). Data Summary, USGS, USA
Gautier M, Gharbi K, Cezard T, Foucaud J, Kerdelhué C, Pudlo P, Cornuet JM, Estoup A (2013) The effect of RAD allele dropout on the estimation of genetic variation within and between populations. Mol Ecol 22:3165–3178. https://doi.org/10.1111/mec.12089
Granato ISC, Galli G, de Oliveira Couto EG, Bandeira e Souza M, Freitas Mendonça F, Fritsche-Neto R (2018) SnpReady: a tool to assist breeders in genomic analysis. Mol Breeding 38:102. https://doi.org/10.1007/s11032-018-0844-8
Hammond TT, Curtis MJ, Jacobs LE, Gaffney PM, Clancy MM, Swaisgood RR, Shier DM (2021) Overwinter behavior movement and survival in a recently reintroduced endangered amphibian Rana muscosa. J Nat Conserv 64:126086. https://doi.org/10.1016/j.jnc.2021.126086
Hare MP, Nunney L, Schwartz MK et al (2011) Understanding and estimating effective population size for practical application in marine species management. Conserv Biol 25:438–449. https://doi.org/10.1111/j.1523-1739.2010.01637.x
Hartl DL, Clark GC (1997) Principles of population genetics. Sinauer Associates, Sunderland
Hayes TB, Collins A, Lee M, Mendoza M, Noriega N, Stuart AA, Vonk A (2002) Hermaphroditic demasculinized frogs after exposure to the herbicide atrazine at low ecologically relevant doses. Proc Natl Acad Sci USA 99:5476–5480. https://doi.org/10.1073/pnas.082121499
Hinkson KM, Henry NL, Hensley NM, Richter SC (2016) Initial founders of captive populations are genetically representative of natural populations in critically endangered dusky gopher frogs, Lithobates sevosus. Zoo Biol 35:378–384. https://doi.org/10.1002/zoo.21309
Hogg JT, Forbes SH, Steele BM, Luikart G (2006) Genetic rescue of an insular population of large mammals. Proc Royal Society B 273:1491–1499. https://doi.org/10.1098/rspb.2006.3477
Hogg CJ, Wright B, Morris KM, Lee AV, Ivy JA, Grueber CE, Belov K (2019) Founder relationships and conservation management: empirical kinships reveal the effect on breeding programmes when founders are assumed to be unrelated. Anim Conserv 22:348–361. https://doi.org/10.1111/acv.12463
Hon T, Mars K, Young GY-C et al (2020) Highly accurate long-read HiFi sequencing data for five complex genomes. Sci Data 7:399. https://doi.org/10.1038/s41597-020-00743-4
Howell LG, Frankham R, Rodger JC, Witt RR, Clulow S, Upton RMO, Clulow J (2021a) Integrating biobanking minimises inbreeding and produces significant cost benefits for a threatened frog captive breeding programme. Conserv Lett 14:e12776. https://doi.org/10.1111/conl.12776
Howell LG, Mawson PR, Frankham R et al (2021b) Integrating biobanking could produce significant cost benefits and minimise inbreeding for Australian amphibian captive breeding programs. Reprod Fert Develop 33:573–587. https://doi.org/10.1071/RD21058
IUCN SSC Amphibian Specialist Group (2022). Rana muscosa. IUCN Red List of Threatened Species. e.T19177A118975294.
Ivy JA, Lacy RC (2012) A comparison of strategies for selecting breeding pairs to maximize genetic diversity retention in managed populations. J Hered 103:186–196. https://doi.org/10.1093/jhered/esr129
Ivy JA, Putnam AS, Navarro AY, Gurr J, Ryder OA (2016) Applying SNP-derived molecular coancestry estimates to captive breeding programs. J Hered 107:403–412. https://doi.org/10.1093/jhered/esw029
Jakobsson M, Rosenberg NA (2007) Clumpp: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806. https://doi.org/10.1093/bioinformatics/btm233
Jamieson IG (2015) Significance of population genetics for managing small natural and reintroduced populations in New Zealand. New Zeal J Ecol 39:1–18
Johnson WE, Onorato DP, Roelke ME (2010) Genetic restoration of the Florida panther. Science 24:1641–1645. https://doi.org/10.1126/science.1192891
Johnson K, Baker A, Buley K, Carrillo L, Gibson R, Gillespie GR et al (2020) A process for assessing and prioritizing species conservation needs: going beyond the Red List. Oryx 54:125–132. https://doi.org/10.1017/S0030605317001715
Jones KL, Glenn TC, Lacy RC, Pierce JR, Unruh N, Mirande CM, Chavez-Ramirez F (2002) Refining the whooping crane studbook by incorporating microsatellite dna and leg-banding analyses. Conserv Biol 16:789–799. https://doi.org/10.1046/j.1523-1739.2002.00001.x
Kats LB, Ferrer RP (2003) Alien predators and amphibian declines: review of two decades of science and the transition to conservation. Divers Distrib 9:99–110. https://doi.org/10.1046/j.1472-4642.2003.00013.x
Kiesecker JM, Blaustein AR, Belden LK (2001) Complex causes of amphibian population declines. Nature 410:681–684. https://doi.org/10.1038/35070552
Koepfli KP, Paten B, Genome 10K Community of Scientists, O’Brien SJ (2015) The Genome 10K Project: a way forward. Annu Rev Anim Biosci 3:57–111. https://doi.org/10.1146/annurev-animal-090414-014900
Kouba AJ, Lloyd RE, Houck ML et al (2013) Emerging trends for biobanking amphibian genetic resources: the hope reality and challenges for the next decade. Biol Conserv 164:10–21. https://doi.org/10.1016/j.biocon.2013.03.010
Kupferberg SJ, Palen WJ, Lind AJ, Bobzien S, Catenazzi A, Drennan J, Power ME (2012) Effects of flow regimes altered by dams on survival, population declines, and range-wide losses of California river-breeding frogs. Conserv Biol 26:513–524
Lacy RC (1995) Clarification of genetic terms and their use in the management of captive populations. Zoo Biol 14:565–577. https://doi.org/10.1002/zoo.1430140609
Lacy RC, Ballou JD, Princée F, Starfield A, Thompson EA (1995) Pedigree analysis for population management. In: Ballou JD, Gilpin M, Foose TJ (eds) Population management for survival and recovery. Analytical methods and strategies in small population conservation. Columbia University Press, New York, pp 57–75
Lacy RC, Ballou JD, Pollak JP (2012) PMx: software package for demographic and genetic analysis and management of pedigreed populations. Methods Ecol Evol 3:433–437
Lemopoulos A, Prokkola JM, Uusi-Heikkilä S et al (2019) Comparing RADseq and microsatellites for estimating genetic diversity and relatedness—Implications for brown trout conservation. Ecol Evol 9:2106–2120. https://doi.org/10.1002/ece3.4905
Li Q, Guo Q, Zhou Y et al (2020) A draft genome assembly of the eastern banjo frog Limnodynastes dumerilii dumerilii (Anura: Limnodynastidae). Gigabyte. https://doi.org/10.46471/gigabyte.2
Liedtke HC, Gower DJ, Wilkinson M et al (2018) Macroevolutionary shift in the size of amphibian genomes and the role of life history and climate. Nat Ecol Evol 2:1792–1799. https://doi.org/10.1038/s41559-018-0674-4
Lynch M (1988) Design and analysis of experiments on random drift and inbreeding depression. Genetics 120:791–807. https://doi.org/10.1093/genetics/120.3.791
Lynch M, Ritland K (1999) Estimation of pairwise relatedness with molecular markers. Genetics 152:1753–1766. https://doi.org/10.1093/genetics/152.4.1753
Madsen T, Shine R, Olsson M, Wittzell H (1999) Restoration of an inbred adder population. Nature 402:34–35. https://doi.org/10.1038/46941
Marsh DM, Trenham PC (2001) Metapopulation dynamics and amphibian conservation. Conserv Biol 15:40–49. https://doi.org/10.1111/j.1523-1739.2001.00129.x
Miller-Butterworth CM, Vacco K, Russell AL, Gaspard JC (2021) Genetic diversity and relatedness among captive African painted dogs in North America. Genes 12:1463. https://doi.org/10.3390/genes12101463
Paris JR, Stevens JR, Catchen JM (2017) Lost in parameter space: a road map for stacks. Methods Ecol Evol 8:1360–1373. https://doi.org/10.1111/2041-210X.12775
Peek RA, Sean MOR, Miller MR (2021) Flow modification associated with reduced genetic health of a river-breeding frog Rana boylii. Ecosphere 12:e03496. https://doi.org/10.1002/ecs2.3496
Poorten TJ, Knapp RA, Rosenblum EB (2017) Population genetic structure of the endangered Sierra Nevada yellow-legged frog (Rana Sierrae) in Yosemite National Park based on multi-locus nuclear data from swab samples. Conserv Genet 18:731–744. https://doi.org/10.1007/s10592-016-0923-5
Pounds A, Fogden M, Campbell J (1999) Biological response to climate change on a tropical mountain. Nature 398:611–614. https://doi.org/10.1038/19297
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959. https://doi.org/10.1093/genetics/155.2.945
Raj A, Stephens M, Pritchard JK (2014) fastSTRUCTURE: variational inference of population structure in large SNP data sets. Genetics 197:573–589. https://doi.org/10.1534/genetics.114.164350
Ralls K, Ballou J (1986) Captive breeding programs for populations with a small number of founders. Trends Ecol Evol 1:19–22. https://doi.org/10.1016/0169-5347(86)90062-5
Rogers SD, Peacock MM (2012) The disappearing northern leopard frog (Lithobates pipiens): conservation genetics and implications for remnant populations in western Nevada. Ecol Evol 2:2040–2056. https://doi.org/10.1002/ece3.308
Ryan ME, Palen WJ, Adams MJ, Rochefort RM (2014) Amphibians in the climate vise: loss and restoration of resilience of montane wetland ecosystems in the western US. Front Ecol Environ 12:232–240. https://doi.org/10.1890/130145
Sambrook J, Fritsch JEF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York
Sandoval-Castillo J, Attard CRM, Marri S, Brauer CJ, Möller LM, Beheregaray LB (2017) Swinger: a user-friendly computer program to establish captive breeding groups that minimize relatedness without pedigree information. Mol Ecol Resour 17:278–287. https://doi.org/10.1111/1755-0998.12609
Savage AE, Zamudio KR (2011) MHC genotypes associate with resistance to a frog-killing fungus. Proc Natl Acad Sci USA 108:16705–16710. https://doi.org/10.1073/pnas.1106893108
Scheele BC, Pasmans F, Skerratt LF et al (2019) Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity. Science 363:1459–1463. https://doi.org/10.1126/science.aav0379
Schoville SD, Tustall TS, Vredenburg VT, Backlin AR, Gallegos E, Wood AR, Fisher RN (2011) Conservation genetics of evolutionary lineages of the endangered mountain yellow-legged frog Rana muscosa (Amphibia: Ranidae) in southern California. Biol Conserv 14:2031–2040. https://doi.org/10.1016/j.biocon.2011.04.025
Shaffer HB, Gidiş M, McCartney-Melstad E, Neal KM, Oyamaguchi HM, Tellez M, Toffelmier EM (2015) Conservation genetics and genomics of amphibians and reptiles. Annu Rev Anim Biosci 3:113–138. https://doi.org/10.1146/annurev-animal-022114-110920
Silla AJ, Calatayud NE, Trudeau VL (2021) Amphibian reproductive technologies: approaches and welfare considerations. Conserv Physiol 9:coab011. https://doi.org/10.1093/conphys/coab011
Thompson ME, Nowakowski AJ, Donnelly MA (2016) The importance of defining focal assemblages when evaluating amphibian and reptile responses to land use. Conserv Biol 30:249–258. https://doi.org/10.1111/cobi.12637
U.S. Fish & Wildlife Service (2023) Mountain yellow-legged frog (Rana muscosa). Environmental Conservation Online System.
Valbuena-Ureña E, Soler-Membrives A, Steinfartz S (2017) Getting off to a good start? Genetic evaluation of the ex situ conservation project of the critically endangered montseny brook newt (Calotriton arnoldi). PeerJ 5:e3447. https://doi.org/10.7717/peerj.3447
VanRaden PM (2008) Efficient methods to compute genomic predictions. J Dairy Sci 91:4414–4423. https://doi.org/10.3168/jds.2007-0980
Vredenburg VT (2004) Reversing introduced species effects: experimental removal of introduced fish leads to rapid recovery of declining frog. Proc Natl Acad Sci USA 101:7646–7650. https://doi.org/10.1073/pnas.0402321101
Wang J (2007) Triadic IBD coefficients and applications to estimating pairwise relatedness. Genet Res 89:135–153. https://doi.org/10.1017/S0016672307008798
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370. https://doi.org/10.2307/2408641
Weisrock DW, Hime PM, Nunziata SO et al (2018) Surmounting the large-genome “problem” for genomic data generation in salamanders. In: Hohenlohe PA, Rajora OP (eds) Population genomics: wildlife. Population genomics. Springer, Cham, pp 115–142. https://doi.org/10.1007/13836_2018_36
Westemeier RL, Brawn JD, Simpson SA et al (1998) Tracking the long-term decline and recovery of an isolated population. Science 282:1695–1698. https://doi.org/10.1126/science.282.5394.1695
Whiteley RA, Fitzpatrick SW, Funk WC, Tallmon DA (2015) Genetic rescue to the rescue. Trends Ecol Evol 30:42–49. https://doi.org/10.1016/j.tree.2014.10.009
Wilber M, Johnson P, Briggs C (2019) When chytrid fungus invades: integrating theory and data to understand disease-induced amphibian declines. In: Wilson K, Fenton A, Tompkins D (eds) Wildlife disease ecology: linking theory to data and application. Cambridge University Press, Cambridge, pp 511–543. https://doi.org/10.1017/9781316479964.018
Wilder AP, Navarro AY, King SND et al (2020) Fitness costs associated with ancestry to isolated populations of an endangered species. Conserv Genet 21:589–601. https://doi.org/10.1007/s10592-020-01272-8
Wildt D, Miller P, Koepfli K-P, Pukazhenthi B, Palfrey K, Livingston G, Beetem D, Shurter S, Gregory J, Takács M, Snodgrass K (2019) Breeding centers, private ranches, and genomics for creating sustainable wildlife populations. Bioscience 69:928–943. https://doi.org/10.1093/biosci/biz091
Willis K, Lacy RC (2016) Use of animals with partially known ancestries in scientifically managed breeding programs. Zoo Biol 35:319–325. https://doi.org/10.1002/zoo.21295
Wilson GA, Fulton TL, Kendell K, Scrimgeour G, Paszkowski CA, Coltman DW (2008) Genetic diversity and structure in Canadian northern leopard frog (Rana pipiens) populations: implications for reintroduction programs. Can J Zool 86:863–874. https://doi.org/10.1139/Z08-062
Wright S (1978) Evolution and the genetics of populations, vol 4. University of Chicago Press, Chicago
Acknowledgements
We would like to thank our partners in the R. muscosa recovery program including the United States Fish and Wildlife Service, California Department of Fish and Wildlife, United States Forest Service, United States Geological Survey (USGS), the Los Angeles Zoo, Omaha’s Henry Doorly Zoo, University of California, Los Angeles, Aquarium of the Pacific and Santa Ana Zoo. We appreciate the support of Jonathan Richmond and Robert Fisher from USGS, for providing the San Gabriel DNA samples used as reference population in this study. Finally, and most importantly, we acknowledge that our research takes place on the traditional lands of numerous Indigenous Peoples. We would therefore like to respectfully acknowledge the traditional custodians of the land on which this work was conducted and pay our respect to Elders both past, present and emerging.
Funding
This work was supported by the Disney Conservation Fund AZA/AZH (Conservation Grants Funds File Number: 17-1433). Dr. Calatayud received financial aid from Exploradora de Immuebles, S.A. (EISA) as postdoctoral fellow.
Author information
Authors and Affiliations
Contributions
CCS, JI, NEC and DMS contributed to the study conception and design. Material preparation, data collection and analysis were performed by CCS, LJ, EC, AW and JI. The first draft of the manuscript was written by CCS and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Competing Interests
The authors have no conflicts of interest nor relevant financial/non-financial interests to disclose that are relevant to the content of this article.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Steiner, C.C., Jacobs, L., Choi, E. et al. Integrating genomics into the genetic management of the endangered mountain yellow-legged frog. Conserv Genet 25, 647–662 (2024). https://doi.org/10.1007/s10592-023-01594-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-023-01594-3