Temporal stability in color patterns and body size variation in a six-year monitored population of the aposematic toad (Melanophryniscus rubriventris)
Evolutionary Ecology - Trang 1-13
Tóm tắt
Color polymorphisms in poison frogs have intrigued evolutionary ecologists, as understanding the mechanisms that sustain them is of great interest. Temporal variation in selection is considered crucial for maintaining color polymorphism, and monitoring aposematic signals provides valuable insights into such temporal dynamics. We conducted a six-year study on red-belly toads, Melanophryniscus rubriventris, analyzing color patterns and body size variation across five reproductive seasons. Our findings show stable color morph ratios over time, with no discernible differences between sexes and no interdependence between dorsal and ventral patterns. Notably, darker morphs, mostly melanic, comprised only about 25% of the population, contrasting with the higher frequency of conspicuous aposematic combinations. Intermediate morphs were more prevalent, while the most extreme conspicuous dorsal pattern was rare. Regarding body size, females were significantly larger and in better body condition than males. We observed a significant decrease in snout-vent length for males between 2021 and 2022, while females showed a significant increase between 2020 and 2022. Interestingly, there was a phenotypic association between color patterns and body size, with males exhibiting black bellies having smaller snout-vent lengths compared to those with other ventral patterns, particularly red bellies. Our study suggests that dorsal and ventral color patterns may respond differently to selection. The stability of color patterns within the population could be upheld through complex interactions involving stabilizing and sexual selection. We emphasize the importance of long-term studies and recommend that future research considers reproductive ecology and individual behavioral decisions in this polymorphic aposematic species. By incorporating these aspects, we can gain a more comprehensive understanding of the mechanisms driving phenotypic variation.
Tài liệu tham khảo
citation_journal_title=Q Rev Biol; citation_title=The evolution of body size: what keeps organisms small?; citation_author=WU Blackenhorn; citation_volume=75; citation_publication_date=2000; citation_pages=385-407; citation_doi=10.1086/393620; citation_id=CR1
citation_journal_title=Evolution; citation_title=Adaptive phenotypic plasticity in growth, development, and body size in the yellow dung fly; citation_author=WU Blanckenhorn; citation_volume=52; citation_publication_date=1998; citation_pages=1394-1407; citation_doi=10.2307/2411309; citation_id=CR2
citation_journal_title=J Herpetol; citation_title=Geographic variation of the diet of Melanophryniscus rubriventris (Anura: Bufonidae) in Northwestern Argentina; citation_author=MI Bonansea, M Vaira; citation_volume=41; citation_publication_date=2007; citation_pages=230-236; citation_doi=10.1670/0022-1511(2007)41[231:GVOTDO]2.0.CO;2; citation_id=CR3
citation_journal_title=Amphib-Reptil; citation_title=Geographic and intrapopulational variation in colour and patterns of an aposematic toad, Melanophryniscus rubriventris (Amphibia, Anura, Bufonidae); citation_author=MI Bonansea, M Vaira; citation_volume=33; citation_publication_date=2012; citation_pages=11-24; citation_doi=10.1163/156853811X619754; citation_id=CR4
citation_journal_title=PLoS Biol; citation_title=Bigger is fitter? Quantitative genetic decomposition of selection reveals an adaptive evolutionary decline of body mass in a wild rodent population; citation_author=T Bonnet, P Wandeler, G Camenisch, E Postma; citation_volume=15; citation_publication_date=2017; citation_pages=e1002592; citation_doi=10.1371/journal.pbio.1002592; citation_id=CR5
Bosch J, Mestre J, Baiges C, Martínez JE, Calvo JF, Jiménez‐Franco MV (2019) Colour plumage polymorphism in the Booted Eagle: inheritance pattern and temporal stability of the morph frequencies. J Zool 308:212–220
citation_journal_title=Evolution; citation_title=Geographic variation, frequency-dependent selection, and the maintenance of a female-limited polymorphism; citation_author=B Calsbeek, L Bonvini, RM Cox; citation_volume=64; citation_publication_date=2009; citation_pages=116-125; citation_doi=10.1111/j.1558-5646.2009.00808.x; citation_id=CR6
citation_journal_title=J Zool; citation_title=Melanism, body condition and elevational distribution in the asp viper; citation_author=B Castella, J Golay, JC Monney, P Golay, K Mebert, S Dubey; citation_volume=290; citation_publication_date=2013; citation_pages=273-280; citation_doi=10.1111/jzo.12037; citation_id=CR7
citation_journal_title=Mol Phylogenet Evol; citation_title=Phytogeographic patterns and cryptic diversity in an aposematic toad from NW Argentina; citation_author=RB Clemente-Carvalho, M Vaira, LE King, D Koscinski, MI Bonansea, SC Lougheed; citation_volume=116; citation_publication_date=2017; citation_pages=248-256; citation_doi=10.1016/j.ympev.2017.07.013; citation_id=CR8
citation_journal_title=Bull Chic Herpetol Soc; citation_title=Why the striking diversity of conspicuous color patterns in a poison frog from Central America?; citation_author=JL Coleman; citation_volume=58; citation_publication_date=2023; citation_pages=70-74; citation_id=CR9
citation_journal_title=Proc Natl Acad Sci USA; citation_title=Selective loss of polymorphic mating types is associated with rapid phenotypic evolution during morphic speciation; citation_author=A Corl, AR Davis, SR Kuchta, B Sinervo; citation_volume=107; citation_publication_date=2010; citation_pages=4254-4259; citation_doi=10.1073/pnas.0909480107; citation_id=CR10
citation_journal_title=J Nat Hist; citation_title=Spatial and temporal dynamics of exuberant colour polymorphism in the southern cricket frog; citation_author=CL Cox, J Bowers, C Obialo, JD Curlis, JW Streicher; citation_volume=54; citation_publication_date=2021; citation_pages=2249-2264; citation_doi=10.1080/00222933.2020.1842536; citation_id=CR11
citation_journal_title=J Chem Ecol; citation_title=Alkaloids in bufonid toads (Melanophryniscus): temporal and geographic determinants for two Argentinian species; citation_author=JW Daly, JM Wilham, TF Spande, HM Garrafo, RR Gil, GL Silva, M Vaira; citation_volume=33; citation_publication_date=2007; citation_pages=871-887; citation_doi=10.1007/s10886-007-9261-x; citation_id=CR12
citation_journal_title=Evolution; citation_title=Heterozygote advantage and pleiotropy contribute to intraspecific color trait variability; citation_author=C Pasqual, K Suisto, J Kirvesoja, S Gordon, T Ketola, J Mappes; citation_volume=76; citation_publication_date=2022; citation_pages=2389-2403; citation_doi=10.1111/evo.14597; citation_id=CR13
citation_journal_title=Heredity; citation_title=Heritability of plumage colour morph variation in a wild population of promiscuous, long-lived Australian magpies; citation_author=AE Dobson, DJ Schmidt, JM Hughes; citation_volume=123; citation_issue=3; citation_publication_date=2019; citation_pages=349-358; citation_doi=10.1038/s41437-019-0212-4; citation_id=CR14
citation_journal_title=BMC Evol Biol; citation_title=Diversifying selection and color-biased dispersal in the asp viper; citation_author=S Dubey, V Zwahlen, K Mebert, JC Monney, P Golay, T Ott, T Durand, G Thiery, L Kaiser, SN Geser, S Ursenbacher; citation_volume=15; citation_publication_date=2015; citation_pages=1-9; citation_doi=10.1186/s12862-015-0367-4; citation_id=CR15
citation_journal_title=Trends Ecol Evol; citation_title=Pleiotropy in the melanocortin system, coloration and behavioural syndromes; citation_author=AL Ducrest, L Keller, A Roulin; citation_volume=23; citation_publication_date=2008; citation_pages=502-510; citation_doi=10.1016/j.tree.2008.06.001; citation_id=CR16
citation_journal_title=Philos Trans R Soc Lond B; citation_title=Frequency-dependent predation, crypsis and aposematic coloration; citation_author=JA Endler; citation_volume=319; citation_publication_date=1988; citation_pages=505-523; citation_doi=10.1098/rstb.1988.0062; citation_id=CR17
citation_title=Evolutionary implications of the interaction between animal signals and the environment; citation_inbook_title=Animal signals: signalling and signal design in animal communication; citation_publication_date=2000; citation_pages=11-46; citation_id=CR18; citation_author=JA Endler; citation_publisher=Tapir Academic Press
García CG (2018) Estrategias reproductivas y conflicto sexual en Melanophryniscus rubriventris, un anuro con reproducción explosiva. PHD manuscript.
https://ri.conicet.gov.ar/handle/11336/95783
.
citation_journal_title=Springerplus; citation_title=Alkaloids from single skin of the Argentinian toad Melanophryniscus rubriventris (Anura: Bufonidae): an unexpected variability in alkaloid profiles and a profusion of new structures; citation_author=HM Garrafo, NR Andriamaharavo, M Vaira, MF Quiroga, C Heit, TF Spande; citation_volume=1; citation_publication_date=2012; citation_pages=51; citation_doi=10.1186/2193-1801-1-51; citation_id=CR20
citation_journal_title=Can J Zool; citation_title=Oviposition-site selection by the toad Melanophryniscus rubriventris in an unpredictable environment in Argentina; citation_author=F Goldberg, S Quinzio, M Vaira; citation_volume=84; citation_publication_date=2006; citation_pages=699-705; citation_doi=10.1139/z06-038; citation_id=CR21
citation_journal_title=J Anim Ecol; citation_title=Colour polymorphism torn apart by opposing positive frequency-dependent selection, yet maintained in space; citation_author=SP Gordon, H Kokko, B Rojas, O Nokelainen, J Mappes; citation_volume=84; citation_publication_date=2015; citation_pages=1555-1564; citation_doi=10.1111/1365-2656.12416; citation_id=CR22
citation_journal_title=Trends Ecol Evol; citation_title=Linking color polymorphism maintenance and speciation; citation_author=SM Gray, JS McKinnon; citation_volume=22; citation_publication_date=2007; citation_pages=71-79; citation_doi=10.1016/j.tree.2006.10.005; citation_id=CR23
citation_journal_title=Sci Rep; citation_title=Rapid phenotypic change in a polymorphic salamander over 43 years; citation_author=MM Hantak, NA Federico, DC Blackburn, RP Guralnick; citation_volume=11; citation_publication_date=2021; citation_pages=22681; citation_doi=10.1038/s41598-021-02124-2; citation_id=CR24
citation_journal_title=J Heredity; citation_title=Heterozygote advantage in a finite population: black color in wolves; citation_author=PW Hedrick, DR Stahler, D Dekker; citation_volume=105; citation_publication_date=2014; citation_pages=457-465; citation_doi=10.1093/jhered/esu024; citation_id=CR25
citation_journal_title=Evolution; citation_title=Negative-assortative mating for color in wolves; citation_author=PW Hedrick, DW Smith, DR Stahler; citation_volume=70; citation_publication_date=2016; citation_pages=757-766; citation_doi=10.1111/evo.12906; citation_id=CR26
citation_journal_title=J Evol Biol; citation_title=Predator response to the coloured eyespots and defensive posture of Colombian four-eyed frogs; citation_author=TL Hernández-Palma, LA Rueda-Solano, JK Valkonen, B Rojas; citation_publication_date=2023; citation_doi=10.1111/jeb.14193; citation_id=CR27
citation_journal_title=Phil Trans Royal Soc B: Biol Sci; citation_title=Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation; citation_author=RB Huey, MR Kearney, A Krockenberger, JA Holtum, M Jess, SE Williams; citation_volume=367; citation_publication_date=2012; citation_pages=1665-1679; citation_doi=10.1098/rstb.2012.0005; citation_id=CR28
citation_journal_title=Nature; citation_title=Accelerated speciation in colour-polymorphic birds; citation_author=AF Hugall, D Stuart-Fox; citation_volume=485; citation_issue=7400; citation_publication_date=2012; citation_pages=631-634; citation_doi=10.1038/nature11050; citation_id=CR29
citation_journal_title=Nature; citation_title=Mating advantage for rare males in wild guppy populations; citation_author=KA Hughes, AE Houde, AC Price, FH Rodd; citation_volume=503; citation_publication_date=2013; citation_pages=108-110; citation_doi=10.1038/nature12717; citation_id=CR30
citation_journal_title=Science; citation_title=Adaptive introgression underlies polymorphic seasonal camouflage in snowshoe hares; citation_author=MR Jones, LS Mills, PC Alves, CM Callahan, JM Alves, DJ Lafferty, FM Jiggings, JD Jensen, JM Ferreira, JM Good; citation_volume=360; citation_issue=6395; citation_publication_date=2018; citation_pages=1355-1358; citation_doi=10.1126/science.aar5273; citation_id=CR31
citation_journal_title=Anim Behav; citation_title=Body size predicts between-individual differences in exploration behaviour in the southern corroboree frog; citation_author=SR Kelleher, AJ Silla, NJ Dingemanse, PG Byrne; citation_volume=129; citation_publication_date=2017; citation_pages=161-170; citation_doi=10.1016/j.anbehav.2017.05.013; citation_id=CR32
citation_journal_title=Proc Royal Soc B Biol Sci; citation_title=Evolution of frequency-dependent mate choice: keeping up with fashion trends; citation_author=H Kokko, MD Jennions, A Houde; citation_volume=274; citation_publication_date=2007; citation_pages=1317-1324; citation_doi=10.1098/rspb.2007.0043; citation_id=CR33
citation_journal_title=Evolution; citation_title=Maladaptive mate choice maintained by heterozygote advantage; citation_author=O Krüger, J Lindström, W Amos; citation_volume=55; citation_publication_date=2001; citation_pages=1207-1214; citation_id=CR34
citation_journal_title=Proc Natl Acad Sci; citation_title=Weak warning signals can persist in the absence of gene flow; citation_author=JP Lawrence, B Rojas, A Fouquet, J Mappes, A Blanchette, RA Saporito, RJ Bosquea, EA Courtoise, BP Noonana; citation_volume=116; citation_publication_date=2019; citation_pages=19037-19045; citation_doi=10.1073/pnas.1901872116; citation_id=CR35
citation_journal_title=Trends in Ecol Evol; citation_title=The complex business of survival by aposematism; citation_author=J Mappes, N Marples, JA Endler; citation_volume=20; citation_publication_date=2005; citation_pages=598-603; citation_doi=10.1016/j.tree.2005.07.011; citation_id=CR36
citation_journal_title=J Thermal Biol; citation_title=Does thermal biology differ between two colour pattern morphs of a widespread Australian lizard?; citation_author=JEF Matthews, CR White, DG Chapple; citation_volume=114; citation_publication_date=2023; citation_pages=103579; citation_doi=10.1016/j.jtherbio.2023.103579; citation_id=CR37
citation_journal_title=Mol Ecol; citation_title=Colour polymorphism and correlated characters: genetic mechanisms and evolution; citation_author=JS McKinnon, MER Pierotti; citation_volume=19; citation_publication_date=2010; citation_pages=5101-5125; citation_doi=10.1111/j.1365-294X.2010.04846.x; citation_id=CR38
citation_journal_title=Biol Rev; citation_title=Geographic variation in animal colour polymorphisms and its role in speciation; citation_author=CA McLean, D Stuart-Fox; citation_volume=89; citation_publication_date=2014; citation_pages=860-873; citation_doi=10.1111/brv.12083; citation_id=CR39
citation_journal_title=J Evol Biol; citation_title=Beyond morphs: Inter-individual colour variation despite strong genetic determinism of colour morphs in a wild bird; citation_author=MC Mould, M Huet, L Senegas, B Milá, C Thébaud, Y Bourgeois, AS Chaine; citation_volume=36; citation_publication_date=2023; citation_pages=82-94; citation_doi=10.1111/jeb.14124; citation_id=CR40
citation_journal_title=Biol J Linn Soc; citation_title=Discordance in body size, colour patterns, and advertisement call across genetically distinct populations in a Neotropical anuran (Dendropsophus ebraccatus); citation_author=ME Ohmer, JM Robertson, KR Zamudio; citation_volume=97; citation_publication_date=2009; citation_pages=298-313; citation_doi=10.1111/j.1095-8312.2009.01210.x; citation_id=CR41
citation_journal_title=Evolution; citation_title=Genetic drift within a protected polymorphism: enigmatic variation in color-morph frequencies in the candy-stripe spider, Enoplognatha ovata; citation_author=GS Oxford; citation_volume=59; citation_publication_date=2005; citation_pages=2170-2184; citation_id=CR42
citation_journal_title=Annual Rev Entomol; citation_title=Evolution and ecology of spider coloration; citation_author=GS Oxford, RG Gillespie; citation_volume=43; citation_publication_date=1998; citation_pages=619-643; citation_doi=10.1146/annurev.ento.43.1.619; citation_id=CR43
citation_journal_title=Oikos; citation_title=New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method; citation_author=J Peig, AJ Green; citation_volume=118; citation_publication_date=2009; citation_pages=1883-1891; citation_doi=10.1111/j.1600-0706.2009.17643.x; citation_id=CR44
citation_journal_title=Funct Ecol; citation_title=The paradigm of body condition: a critical reappraisal of current methods based on mass and length; citation_author=J Peig, AJ Green; citation_volume=24; citation_publication_date=2010; citation_pages=1323-1332; citation_doi=10.1111/j.1365-2435.2010.01751.x; citation_id=CR45
citation_journal_title=Evolution; citation_title=Selection on heritable seasonal phenotypic plasticity of body mass; citation_author=F Pelletier, D Réale, D Garant, DW Coltman, M Festa-Bianchet; citation_volume=61; citation_publication_date=2007; citation_pages=1969-1979; citation_doi=10.1111/j.1558-5646.2007.00160.x; citation_id=CR46
citation_journal_title=Can J Zool; citation_title=Diurnal? Calling activity patterns reveal nocturnal habits in the aposematic toad Melanophryniscus rubriventris; citation_author=LC Pereyra, MS Akmentins, EA Sanabria, M Vaira; citation_volume=94; citation_publication_date=2016; citation_pages=497-503; citation_doi=10.1139/cjz-2015-0197; citation_id=CR47
citation_journal_title=Amphib-Reptil; citation_title=Population diet variation and individual specialization in the poison toad, Melanophryniscus rubriventris (Vellard, 1947); citation_author=MF Quiroga, M Vaira, MI Bonansea; citation_volume=32; citation_publication_date=2011; citation_pages=261-265; citation_doi=10.1163/017353710X546530; citation_id=CR48
R Development Core Team (2020) R: a language and environment for statistical computing
Rohlf FJ (2005) tpsDig, digitize landmarks and outlines, version 2.31. Department of Ecology and Evolution, State University of New York at Stony Brook
citation_journal_title=Biol Rev; citation_title=Behavioural, ecological, and evolutionary aspects of diversity in frog colour patterns; citation_author=B Rojas; citation_volume=92; citation_publication_date=2017; citation_pages=1059-1080; citation_doi=10.1111/brv.12269; citation_id=CR51
citation_journal_title=Evol Ecol; citation_title=Sexual dimorphism and intra-populational colour pattern variation in the aposematic frog Dendrobates tinctorius; citation_author=B Rojas, JA Endler; citation_volume=27; citation_publication_date=2013; citation_pages=739-753; citation_doi=10.1007/s10682-013-9640-4; citation_id=CR52
citation_journal_title=Trends Ecol Evol; citation_title=Disruptive selection and then what?; citation_author=C Rueffler, TJ Dooren, O Leimar, PA Abrams; citation_volume=21; citation_publication_date=2006; citation_pages=238-245; citation_doi=10.1016/j.tree.2006.03.003; citation_id=CR53
citation_journal_title=J Therm Biol; citation_title=Variation of thermal parameters in two different color morphs of a diurnal poison toad, Melanophryniscus rubriventris (Anura: Bufonidae); citation_author=E Sanabria, M Vaira, F Quiroga, MS Akmentins, L Pereyra; citation_volume=41; citation_publication_date=2014; citation_pages=1-5; citation_doi=10.1016/j.jtherbio.2014.01.005; citation_id=CR54
citation_journal_title=Behav Ecol; citation_title=Behavioral, energetic, and color trait integration in male guppies: testing the melanocortin hypothesis; citation_author=F Santostefano, KV Fanson, JA Endler, PA Biro; citation_volume=30; citation_publication_date=2019; citation_pages=1539-1547; citation_doi=10.1093/beheco/arz109; citation_id=CR55
citation_journal_title=Herpetol Monogr; citation_title=Developments in amphibian parental care research: history, present advances, and future perspectives; citation_author=LM Schulte, E Ringler, B Rojas, JL Stynoski; citation_volume=34; citation_publication_date=2020; citation_pages=71-97; citation_doi=10.1655/HERPMONOGRAPHS-D-19-00002.1; citation_id=CR56
citation_journal_title=Nature; citation_title=The rock–paper–scissors game and the evolution of alternative male strategies; citation_author=B Sinervo, CM Lively; citation_volume=380; citation_publication_date=1996; citation_pages=240-243; citation_doi=10.1038/380240a0; citation_id=CR57
citation_journal_title=Mol Ecol; citation_title=Back to basics: using colour polymorphisms to study evolutionary processes; citation_author=EI Svensson; citation_volume=26; citation_publication_date=2017; citation_pages=2204-2211; citation_doi=10.1111/mec.14025; citation_id=CR58
citation_journal_title=Am Nat; citation_title=Female polymorphism, frequency dependence, and rapid evolutionary dynamics in natural populations; citation_author=EI Svensson, J Abbott, R Härdling; citation_volume=165; citation_publication_date=2005; citation_pages=567-576; citation_doi=10.1086/429278; citation_id=CR59
citation_journal_title=Evolution; citation_title=Crossing the valley of non-intimidating conspicuousness: evolution of warning coloration through the lens of fitness landscapes; citation_author=A Topper, O Kolodny; citation_volume=77; citation_publication_date=2023; citation_pages=335-341; citation_doi=10.1093/evolut/qpac044; citation_id=CR60
citation_journal_title=Behav Ecol; citation_title=Alternative reproductive strategies in the white-throated sparrow: behavioral and genetic evidence; citation_author=EM Tuttle; citation_volume=14; citation_publication_date=2003; citation_pages=425-432; citation_doi=10.1093/beheco/14.3.425; citation_id=CR61
citation_journal_title=Current Biol; citation_title=Divergence and functional degradation of a sex chromosome-like supergene; citation_author=EM Tuttle, AO Bergland, ML Korody, MS Brewer, DJ Newhouse, P Minx, M Stager, A Betuel, ZA Cheviron, WC Warren, RA Gosner, CN Balakrishnan; citation_volume=26; citation_publication_date=2016; citation_pages=344-350; citation_doi=10.1016/j.cub.2015.11.069; citation_id=CR62
citation_journal_title=Cuad Herpetol; citation_title=Variación de la coloración en poblaciones argentinas de Melanophryniscus rubriventris (Vellard, 1947); citation_author=M Vaira; citation_volume=16; citation_publication_date=2002; citation_pages=151-163; citation_id=CR63
citation_journal_title=Amphib-Reptil; citation_title=Annual variation of breeding patterns of the toad Melanophryniscus rubriventris (Vellard, 1947); citation_author=M Vaira; citation_volume=26; citation_publication_date=2005; citation_pages=193-199; citation_doi=10.1163/1568538054253519; citation_id=CR64
citation_journal_title=Acta Zool Lilloana; citation_title=Un nuevo batracio del Norte Argentino; citation_author=J Vellard; citation_volume=4; citation_publication_date=1947; citation_pages=115-119; citation_id=CR65
citation_journal_title=Trends Ecol Evol; citation_title=The impact of learning on sexual selection and speciation; citation_author=MN Verzijden, C Cate, MR Servedio, GM Kozak, JW Boughman, EI Svensson; citation_volume=27; citation_publication_date=2012; citation_pages=511-519; citation_doi=10.1016/j.tree.2012.05.007; citation_id=CR66
citation_journal_title=Mol Ecol; citation_title=Sexual selection and genetic colour polymorphism in animals; citation_author=M Wellenreuther, EI Svensson, B Hansson; citation_volume=23; citation_publication_date=2014; citation_pages=5398-5414; citation_doi=10.1111/mec.12935; citation_id=CR67
citation_journal_title=Biol J Linn Soc; citation_title=Disentangling composite colour patterns in a poison frog species; citation_author=KC Wollenberg, S Lotters, C Mora-Ferrer, M Veith; citation_volume=93; citation_publication_date=2008; citation_pages=433-444; citation_doi=10.1111/j.1095-8312.2007.00906.x; citation_id=CR68