Role of sexual selection

As discussed before, together with the role of natural selection mediated by predators, sexual selection has been suggested to play an important role in the diversification of aposematic signals in poison-dart frogs. Females show preference for brighter (Maan & Cummings, 2009) and more colourful males (Maan & Cummings, 2008) as well for males of their own population in O. pumilio (Summers et al., 1999; Reynolds & Fitzpatrick, 2007; Maan &

Cummings, 2008). I showed here, that aposematic red and cryptic green morphs have a different pulse rate in the male advertisement call in the northern populations. A significant differentiation in this key sexual signal indicates that the females may potentially select males of their own colour, similarly with what has been observed in the congeneric species O.

pumilio.

5. Conclusion

The present work provides evidence for deep intraspecific divergence in the polymorphic aposematic poison-dart frog Oophaga granulifera. I described the patterns of geographical variation in historical and recent genetic structure and in key phenotypic traits such as morphology and advertisement call. The data here presented all congruently show that the southern and northern lineages identified are clearly diverging and may well represent different species. The phylogeographic reconstruction and the recent population structure indicate that the river Río Térraba is likely to be the geographic barrier between the lineages

that are, therefore, geographically, genetically and phenotypically separated.

As concerned to the recent evolution of colour diversity in O. granulifera, several factors may potentially be involved in the origin and maintenance of this notable differentiation.

Alongside correlation data such as those here presented future research efforts will be necessary to empirically evaluate the effective strength in mating preferences shaping the observed variation in colouration. Moreover, many aspects of dendrobatid ecology, such as actual predator community, prey community and related spatial and temporal variation in the acquired toxicity, will have to be clarified to define a clearer evolutionary scenario explaining the reason of the remarkable colour variation in this aposematic vertebrate.

6. References

Aichinger, M. (1991) Tadpole transport in relation to rainfall, fecundity and body size in five species of poison-dart frogs from Amazonian Peru. Amphibia-Reptilia, 12, 49–55.

Alatalo, R.V. & Mappes, J. (1996) Tracking the evolution of warning signals. Nature, 382, 708–709.

Andersson, S., Örnborg, J. & Andersson, M. (1998) Ultraviolet sexual dimorphism and assortative mating in blue tits. Proceedings of the Royal Society of London series B, 265, 445–450.

Arak, A. (1983) Sexual selection by male-male competition in natterjack toad choruses.

Nature, 306, 261–262.

Arntzen, J.W. & Wallis, G.P. (1999) Geographic variation and taxonomy of crested newts (Triturus cristatus superspecies): morphological and mitochondrial DNA data.

Contributions to Zoology, 68, 181–203.

Auber, L. (1957) The distribution of structural colours and unusual pigments in the class Aves. Ibis, 99, 463–476.

Baeta, R., Faivre, B., Motreuil, S., Gaillard, M. & Moreau, J. (2008) Carotenoid trade-off between parasitic resistance and sexual display: an experimental study in the blackbird (Turdus merula). Proceedings of the Royal Society series B, 275, 427–434.

Bailey, R.I., Thomas, C.D. & Butlin, R.K. (2004) Premating barriers to gene exchange and their implications for the structure of a mosaic hybrid zone between Chorthippus brunneus and C. jacobsi (Orthoptera: Acrididae). Journal of Evolutionary Biology, 17, 108–119.

Barlow, G.W. (1961) Causes and significance of morphological variation in fishes.

Systematic Zoology, 10, 105–117.

Barluenga, M., Stölting, K.N., Salzburger, W., Muschick, M. & Meyer, A. (2006) Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature, 439, 719–723.

Barnett, C.A., Bateson, M. & Rowe, C. (2007) State-dependent decision making: educated predators strategically trade off the costs and benefits of consuming aposematic prey.

Behavioural Ecology, 18, 645–651.

Barton, N. (2004) Speciation: Why, how, where and when? Current Biology, 15, R603–R604.

Beatty, C.D., Beirinck, K. & Sherratt, T.N. (2004) The evolution of Müllerian mimicry in multispecies communities. Nature, 431, 63–67.

Benson, W. (1972) Natural selection for Mullerian mimicry in Heliconius erato in Costa Rica.

Science, 176, 936–939.

Berven, K.A. (1981) Mate choice in the wood frog, Rana sylvatica. Evolution, 35, 707–722.

Berven, K.A. (1982) The genetic basis of altitudinal variation in the wood frog Rana sylvatica. An experimental analysis of life history traits. Evolution, 36, 962–983.

Bezzerides, A.L., McGraw, K.J., Parker, R.S. & Husseini, J. (2007) Elytra color as a signal of chemical defense in the Asian ladybird beetle Harmonia axyridis. Behavioral Ecology and Sociobiology, 61, 1401–1408.

Blair, W.F. (1958) Mating call in the speciation of anuran amphibians. American Naturalist, 92, 27–51.

Blount, J.D., Metcalfe, N.B, Birkhead, T.R & Surai, P.F. (2003) Carotenoid modulation of immune function and sexual attractiveness in zebra finches. Science, 300, 125–127.

Blount, J.D., Speed, M.P, Ruxton, G.D. & Stephens, P.A. (2009) Warning displays may function as honest signals of toxicity. Proceedings of the Royal Society series B, 276, 871–

877.

Bolaños, F. (1990) Actividad de canto y territorialidad en Dendrobates granuliferus. Tesi de maestria, Universidad de Costa Rica.

Brakefield, P.M. & Liebert, T.G. (1985) Studies of colour polymorphism in some marginal populations of the aposematic jersey tiger moth Callimorpha quadripunctaria. Biological Journal of the Linnean Society, 26, 225–241.

Bossuyt, F. & Milinkovitch, M.C. (2000) Convergent adaptive radiations in Madagascan and Asian ranid frogs reveal covariation between larval and adult traits. Proceedings of the National Academy of Sciences USA, 97, 6585–6590.

Bourne, G.R., Collins, A.C., Holder, A.M. & McCarthy, C.L. (2001) Vocal communication and reproductive behavior of the frog Colostethus beebei in Guyana. Journal of Herpetology, 35, 272–281.

Brown, J., Maan, M.E., Cummings, M.E. & Summers, K. (2010) Evidence for selection on coloration in a Panamanian poison frog: a coalescent-based approach. Journal of Biogeography, 37, 891–901.

Caldwell, J.P. (1997) Pair bonding in spotted poison frogs. Nature, 385, 211–214.

Caldwell, J.P., & de Oliveira, V.R.L. (1999) Determinants of biparental care in the spotted poison frog, Dendrobates vanzolinii (Anura: Dendrobatidae). Copeia, 3, 565–575.

Calvert, W.H. (1979) Mortality of the monarch butterfly (Danaus plexippus L.): avian predation at five overwintering sites in Mexico. Science, 204, 847–851.

Camp, D.C., Marshall, J.L., Austin, R.M. Jr. (2000) The evolution of adult body size in black-bellied salamanders (Desmognathus quadramaculatus complex). Canadian Journal of Zoology, 78, 1712–1722.

Campbell, J. (1999) Distribution patterns of amphibians in Middle America. In: Patterns of Distribution of Amphibians (ed. Duellman). The John Hopkins University Press, Baltimore, Maryland.

Campbell, J.A. & Frost, D.R. (1993) Anguid lizards of the genus Abronia: revisionary notes, descriptions of 4 new species, a phylogenetic analysis, and key. Bulletin of the American Museum of Natural History, 1–121.

Carson, H.L. (1975) The genetics of speciation at the diploid level. American Naturalist, 109, 73–92.

Carson, H.L. & Templeton, A.R.A. (1984) Genetic revolutions in relation to speciation phenomena: the founding of new populations. Annual Review of Ecology and Systematics, 15, 97–131.

Castellano, S. & Giacoma, C. (1998) Morphological variation of the green toad, Bufo viridis, in Italy: a test of causation. Journal of Herpetology, 32, 540–550.

Cherry, L.M., Case, S.M. & Wilson, A.C. (1978) Frog perspective on the morphological difference between humans and chimpanzees. Science, 200, 209–211.

Clarke, R.D. (1972) The effect of toe clipping on survival in Fowler's toad (Bufo woodhousei fowleri). Copeia, 1, 182–185.

Clement, M., Posada, D. & Crandall, K.A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657–1659.

Clough, M. & Summers, K. (2000) Phylogenetic systematics and biogeography of the poison frogs: evidence from mitochondrial DNA sequences. Biological Journal of the Linnean Society, 70, 515–540.

Coates, A.C. & Obando, J.A. (1996) The geological evaluation of the Central American Isthmus. In: Evolution and Environment in Tropical America (eds. Jackson, B.C., Budd, A.F. & Coates, A.G.). University of Chicago Press, Chicago. Illinois, 21–56.

Colangelo, P., Castiglia, R., Franchini, P. & Solano E. (2010) Pattern of shape variation in the eastern African gerbils of the genus Gerbilliscus (Rodentia, Muridae): environmental correlations and implication for taxonomy and systematics. Mammalian Biology, 75, 302–

310.

Comeault, A. A. & Noonan, B.P. (2011) Spatial variation in the fitness of divergent aposematic phenotypes of the poison frog, Dendrobates tinctorius. Journal of Evolutionary

Biology, 24, 1374–1379.

Cott, H.B. (1940) Adaptive Coloration in Animals. Methuen, London, UK.

Couldridge, V.C.K & Van Staaden, M.J. (2004) Habitat-dependent transmission of male advertisement calls in bladder grasshoppers (Orthoptera; Pneumoridae). Journal of Experimental Biology, 207, 2777–2786.

Coyne, J. A. (1992) Genetics and speciation. Nature, 355, 511–515.

Crawford, A.J. (2003) Huge populations and old species of Costa Rican and Panamanian dirt frogs inferred from mitochondrial and nuclear gene sequences. Molecular Ecology, 12, 2525–2540.

Crawford, A.J., Bermingham, E. & Polania, C. (2007) The role of tropical dry forest as a long–term barrier to dispersal: a comparative phylogeographical analysis of dry forest tolerant and intolerant frogs. Molecular Ecology, 16, 4789–4807.

Crump, M.L. (1972) Territoriality and mating behaviour in Dendrobates granuliferus (Anura:

Dendrobatidae). Herpetologica, 28, 195–198.

Daly, J.W. & Myers, C.W. (1967) Toxicity of Panamanian poison frogs (Dendrobates): some biological and chemical aspects. Science, 156, 970–973.

Daly, J.W., Myers, C.W. & Whittaker, N. (1987) Further classification of skin alkaloids from neotropical poison frogs (Dendrobatidae), with a general survey of toxic/noxious substances in the Amphibia. Toxicon, 10, 1023–1095.

Daly, J.W., Garraffo, H.M., Spande, T.F., Jaramillo, C. & Rand, A.S. (1994a) Dietary source for skin alkaloids of poison frogs (Dendrobatidae)? Journal of Chemical Ecology, 20, 943–

955.

Daly, J.W., Gusovsky, F., Myers, C.W., Yotsu-Yamashita, M. & T. Yasumoto (1994b) First occurrence of tetrodotoxin in a dendrobatid frog (Colostethus inguinalis), with further reports for the bufonid genus Atelopus. Toxicon, 32, 279–285.

Daly, J.W., Garraffo, H.M. & Myers, C.W. (1997) The origin of frog skin alkaloids: an enigma. Pharmaceutical News, 4, 9–14.

Daly, J.W. (1998) Thirty years of discovering arthropod alkaloids in amphibian skin. Journal of Natural Products, 61, 162–172.

Daly, J.W., Garraffo, H.M. & Spande, T.F. (1999) Alkaloids from amphibian skins. In Alkaloids: chemical and biological perspectives (ed. Pelletier, S.W.). Pergamon, New York, 1–161.

Daly, J.W., Garraffo, H.M. Spande, T.F. Decker, M.W. Sullivan, J.P. & Williams, M. (2000) Alkaloids from frog skins: the discovery of epibatidine and the potential for developing novel non-opioid analgesics. Natural Products Report, 17, 131–135.

Darst, C.R., Cummings, M.E. & Cannatella, D.C. (2006) A mechanism for diversity in warning signals: conspicuousness versus toxicity in poison frogs. Proceedings of the National Academy of Sciences of the USA, 103, 5852–5857.

Darwin C (1859) On the Origin of Species by Means of Natural Selection (John Murray, London).

Dijkstra, P.D., Seehausen, O. & Groothuis, T.G.G. (2008) Intra-sexual competition among females and the stabilization of a conspicuous colour polymorphism in a Lake Victoria cichlid fish. Proceedings of the Royal Society of London Series B, 275, 519–526.

Dobzhansky T. (1940) Speciation as a stage in evolutionary divergence. American Naturalist 74, 312–321.

Doebeli, M. & Dieckmann, U. (2004) Adaptive dynamics of speciation: spatial structure. In:

Adaptive Speciation (eds. Dieckmann, U., Doebeli, M., Metz, J.A.J., Tautz, D.).

Dover, G. (1995) A species definition: a functional approach. Trends in Ecology &

Evolution, 12, 489–490.

Driscoll, D.A. (1998) Genetic structure, metapopulation processes and evolution influence the conservation strategies for two endangered frog species. Biological Conservation, 83, 43–

54.

Duellman, W.E. (2001) The Hylid Frogs of Middle America. Society for the Study of Amphibians and Reptiles, Ithaca, New York.

Dumbacher, J.P., Wako, A., Derrickson, S.R., Samuelson, A., Spande, T.F. & Daly., J.W.

(2004). Melyrid beetles (Choresine): a putative source for the batrachotoxin alkaloids found in poison-dart frogs and toxic passerine birds. Proceedings of the National Academy of Science USA, 101, 15857–15860.

Edmunds, M. (1974) Defence in Animals. A Survey of Anti-Predator Defences. Longman, New York.

Elwood, R., Gibson, J., Neil, S. (1987) The amorous Gammarus: size assortative mating in G.

pulex. Animal Behaviour, 35, 1–6.

Endler, J.A. (1977) Geographic Variation, Speciation and the Origin of Species. Princeton, University Press, Princeton, New Jersey.

Endler, J.A. (1980) Natural selection on color patterns in Poecilia reticulata. Evolution, 34, 76–91.

Endler, J.A. (1983) Natural and sexual selection on colour pattern in poeciliid fishes.

Environmenatl. Biology of Fish, 9, 173–190.

Endler, J.A. (1992) Signals, signal conditions, and the direction of evolution. American Naturalist, 139, 125–153.

Endler, J. & Mappes, J. (2004) Predator mixes and the conspicuousness of aposematic signals.

American Naturalist, 163, 532–547.

Ereshefsky, M. (1992) The Units of Evolution: Essays on the Nature of Species, MIT Press, Cambridge, Massachussetts.

Evanno, G., Regnaut, S. & Goudet, J. (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14, 2611–2620.

Excoffier, L., Smouse, P.E. & Quattro, J.M. (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrlal DNA restriction data. Genetics, 131, 479–491.

Excoffier, L., Laval, G. & Schneider, S. (2005) Arlequin version 3.5: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 1, 47–

60.

Exnerová, A., Landová, E., Stys, P., Fuchs, R., Prokopová, M. & Cehlariková, P. (2003) Reactions of passerine birds to aposematic and non-aposematic firebugs (Pyrrhocorisapterus, Heteroptera). Biological Journal of Linnean Society, 78, 517–525.

Exnerová, A., Stys, P., Fuciková, E., Veselá, S., Svadová, K., Prokopová, M., Jarosık, V., Fuchs, R. & Landová, E. (2007) Avoidance of aposematic prey in European tits (Paridae):

learned or innate? Behavioural Ecology, 18, 148–156.

Fandino, M.C., H. Luddecke & A. Amezquita. (1997) Vocalisation and larval transportation of male Colostethus subpunctatus (Anura: Dendrobatidae). Amphibia-Reptilia, 18, 39–48.

Faulkner, D. J. (1992) Chemical defenses of marine molluscs. In: Ecological Roles of Marine Natural Products (ed. Paul, V. J.). Comstock Publishing Associates, Ithaca, New York, 119–163.

Feder, J.L., Berlocher, S.H., Roethele, J.B., Dambroski, H., Smith, J.J., Perry, W.L., Gavrilovic, V., Filchak, K.E., Rull, J. & Aluja, M. (2003) Allopatric origins for sympatric host-plant shifts and race formation in Rhagoletis. Proceedings of the National Academy of Science USA, 100, 10314–10319.

Feder, J.L., Xie, X., Rull, J., Velez, S., Forbes, A., Dambroski, H., Filchak, K. & Aluja., M.

(2005) Mayr, Dobzhansky, Bush and the complexities of sympatric speciation in Rhagoletis. Proceedings of the National Academy of Science USA, 102, 6573–6580.

Feder, J. L. & Nosil, P. (2009) Chromosomal inversions and species differences: when are genes affecting adaptive divergence and reproductive isolation expected to reside within inversions? Evolution, 63, 3061–3075.

Fink, L.S. & Brower, L.P. (1981) Birds can overcome the cardenolide defense of monarch butterflies in Mexico. Nature, 291, 67–70.

Fisher, D.O. & Cockburn, A. (2006) The large-male advantage in brown antechinuses: female choice, male dominance, and delayed male death. Behavioral Ecology, 17, 164–171.

Fitzpatrick, B.M., Fordyce, J.A. & Gavrilets, S. (2008) What, if anything, is sympatric speciation? Journal of Evolutionary Biology, 21, 1452–1459.

Fitzpatrick, B.M., Fordyce, J.A. & Gavrilets, S. (2009) Pattern, process and geographic modes of speciation. Journal of Evolutionary Biology, 22, 2342–2347.

Forester, D.C. & Czarnowsky, R. (1985) Sexual selection in the spring peeper Hyla crucifer (Amphibia, Anura): role of the advertisement call. Behaviour, 92, 112–128.

Foster, S.A & Endler, J.A. (1999) Geographic variation in behavior: perspectives on evolutionary mechanisms. Oxford University Press, New York.

Frazer, J.F.D. & Rothschild, M. (1960), Defence mechanisms in warningly-coloured moths and other insects Proceedings of the 11th International Congress of Entomology, Vienna, 1959, 249–256.

Friedl, T.W.P. & Klump, G.M. (1997) Some aspects of population biology in the European treefrog, Hyla arborea. Herpetologica, 53, 321–330.

Gabor, C.R., Krenz, J.D. & Jaeger, R.G. (2000) Female choice, male interference, and sperm precedence in the red-spotted newt. Behavioral Ecology, 11, 115–124.

Gabor, C. & Page, R. (2003) Female preference for large males in sailfin mollies, Poecilia latipinna: the importance of predation pressure and reproductive status. Acta ethologica, 6, 7–12.

Gamberale-Stille, G. (2000) Decision time and prey gregariousness influence attack probability in naïve and experienced predators. Animal Behavior, 60, 95–99.

Gamberale-Stille, G. (2001) Benefit by contrast: an experiment with live aposematic prey.

Behavioural Ecology, 12, 768–772.

García-París, M., Good, D.A., Parra-Olea., G. & Wake, D.B. (2000) Biodiversity of Costa Rican salamanders: implications of high levels of genetic differentiation and phylogeographic structure for species formation. Proceedings of the National Academy of Sciences, USA, 97, 1640–1647.

Gavrilets, S. (1997) Evolution and speciation on holey adaptive landscapes. Trends in Ecology and Evolution, 12, 307–312.

Gavrilets, S., Li, H. & Vose, M.D. (2000) Patterns of parapatric speciation. Evolution, 54, 1126–1134.

Gavrilovic, V., Filchak, K.E., Rull, J. & Aluja, M. (2003) Allopatric origins for sympatric host–plant shifts and race formation inRhagoletis. Proceedings of the National Academy of Science USA, 100, 10314–10319.

Gerhardt, H.C. & Huber, F. (2002) Acoustic Communication in Insects and Anurans.

University of Chicago Press, Chicago.

Gittleman, J.L. & Harvey, P.H. (1980) Why are distasteful prey not cryptic? Nature, 286, 149–150.

Golay, N. & Durrer, H. (1994) Inflammation due to toe-clipping in natterjack toads (Bufo calamita). Amphibia-Reptilia, 15, 81–96.

Gomez, D. & Thery, M. (2007) Simultaneous crypsis and conspicuousness in color patterns:

comparative analysis of a neotropical rainforest bird community. American Naturalist, 169, 42–61.

Goodman, D.E. (1971) Territorial behaviour in a neotropical frog, Dendrobates granuliferus.

Copeia, 2, 365–370.

Goudet, J. (1995) FSTAT version 1.2: a computer program to calculate F-statistics. Journal of Heredity, 86, 485–486.

Grant, B.R & Grant, P.R (1989) Evolutionary dynamics of a natural population: the large cactus finch of the Galápagos University of Chicago Press, Chicago, Illinois.

Grant, T., Frost, D.R., Caldwell, J.P., Gagliardo, R., Haddad, C.L., Kok, P.J., Means, D.B., Noonan, B.P., Schargel, W.E. & Wheeler, W.C. (2006) Phylogenetics systematics of dart–poison frogs and their relatives (Amphibia: Athesphatanura: Dendrobatidae).

Bulletin of the American Museum of Natural History, 299, 1–268.

Gray, S.M. & McKinnon, J.S. (2006) Linking color polymorphism maintenance and speciation. Trends in Ecology and Evolution, 22, 71–79.

Green, D.M. (1993) Evolutionary relationships of Eastern Palearctic brown frogs, genus Rana: paraphyly of the 24-chromosome species group and the significance of chromosome number change. Zoological Journal of the Linnean Society, 109, 1–25.

Greenwood, J.J.D., Wood, E.M. & Batchelor, S. (1981) Apostatic selection of distasteful prey. Heredity, 47, 27–34.

Grether, G.F., Hudon, J. & Endler, J.A. (2001) Carotenoid scarcity, synthetic pteridine pigments and the evolution of sexual coloration in guppies (Poecilia reticulata).

Proceedings of the Royal Society series B, 268, 1245–1253.

Griffith, S.C., T.H. Parker & Valérie, A. Olson (2006) Melanin- versus carotenoid-based sexual signals: is the difference really so black and red? Animal Behaviour, 71, 749–763.

Gübitz, T., Thorpe, R.S. & Malhotra, A. (2005) The dynamics of genetic and morphological variation on volcanic islands. Proceedings of the Royal Society of London Series B, 272, 751–757.

Guilford, T. (1986) How do ‘‘warning colors’’ work? Conspicuousness may reduce recognition errors in experienced predators. Animal Behaviour, 34, 286–288.

Guilford, T. (1990) Evolutionary pathways to aposematism. Acta Oecologica, 11, 835–842.

Hagemann, S. & Pröhl, H. (2007) Mitochondrial paraphyly in a polymorphic poison frog species (Dendrobatidae; D. pumilio). Molecular Phylogenetics and Evolution, 45, 740–747.

Hagman, M. & Forsman, A. (2003) Correlated evolution of conspicuous coloration and body size in poison frogs (Dendrobatidae). Evolution, 57, 2904–2910.

Hairston, N.G. (1979) Adaptive significance of color polymorphism in 2 Species of Diaptomus (Copepoda). Limnological Oceanography, 24, 15–37.

Halliday, T. (1996) Amphibians Ecological Census Techniques, A Handbook (ed. Sutherland, W.J.). Cambridge University Press, Cambridge, UK.

Ham, A.D., Ihalainen, E., Lindström, L. & Mappes, J. (2006) Does color matter? The importance of color in avoidance learning, memorability and generalisation. Behavioural Ecology and Sociobiology, 60, 482–491.

Harari, A.R., Handler, A.M. & Landolt, P.J. (1999) Size-assortative mating, male choice and female choice in the curculionid beetle Diaprepes abbreviatus. Animal Behaviour, 58, 1191–1200.

Hartl, D.L. & Clark, A.G. (2007) Principles of Population Genetics, Sinauer, Sunderland, Massachussetts.

Hausdorf, B. (2011) Progress toward a general species concept. Evolution, 65, 923–931.

Hauswaldt, J.S., Ludewig, A.K., Vences, M. & Pröhl, H. (2011) Widespread co-occurrence of divergent mitochondrial haplotype lineages in a Central American species of poison frog (Oophaga pumilio). Journal of Biogeography, 38, 711–726.

Hero, J.M. (1989) A simple code for toe clipping anurans. Herpetological Review, 20, 66–67.

Hill, G.E (1990) Females house finch prefer colourful males: sexual selection for a condition-dependant trait. Animal Behaviour, 40, 563–572.

Hill, G.E. (1993) Geographic variation in the carotenoid plumage pigmentation of male house finches (Carpodacus mexicanus). Biological Journal of the Linnean Society, 49, 63–86.

Hill, G.E. & McGraw, K.J. (2006) Bird Coloration. Vol II. Function and Evolution. Harvard University Press, Cambridge, Massachussetts.

Hodek, I. & Honěk, A. (1996) Ecology of Coccinellidae. Kluwer Academic Publishers, Dordrecht, The Netherlands.

Hoffman, E.A. & Blouin, M.S. (2000) A review of colour and pattern polymorphisms in anurans. Biological Journal of the Linnean Society, 70, 633–665.

Hoffman, E.A., Schueler, F.W., Jones, A.G. & Blouin, M.S. (2006) An analysis of selection on colour polymorphism in the northern leopard frog. Molecular Ecology, 15, 2627–2641.

Hoekstra, H.E., Drumm, K.E. & Nachman, M.W. (2004) Ecological genetics of adaptive color polymorphism in pocket mice: geographic variation in selected and neutral genes.

Evolution, 58, 1329–1341.

Hoekstra, H.E., Krenz, J.G. & Nachman, M.W. (2005) Local adaptation in the rock pocket mouse (Chaetodipus intermedius): natural selection and phylogenetic history of populations. Nature Heredity, 94, 217–228.

Holdridge, L.R. (1947) Determination of world plant formations from simple climatic data.

Science, 105, 367–368.

Humphries, R.B. (1979) Dynamics of a breeding frog community. PhD Thesis. The Australian National University, Canberra, Australia.

Ihalainen, E., Lindström, L. & Mappes, J. (2007) Investigating Müllerian mimicry: predator learning and variation in prey defenses. Journal of Evolutionary Biology, 20, 780–791.

Joron, M. & Mallet, J.L.B. (1998) Diversity in mimicry: paradox or paradigm? Trends in Ecology and Evolution, 13, 461–466.

Juncá, F.A., Altig, R. & Gascon, C. (1994) Breeding biology of Colostethus stepheni, a dendrobatid with a nontrasnported nidicolous tadpole. Copeia, 747–750.

Kapan, D.D. (2001) Three-butterfly system provides a field test of müllerian mimicry. Nature, 409, 338–340.

Kingston, J.L., Rosenthal, G.G. & Ryan, M.J. (2003) The role of sexual selection in maintaining a colour polymorphism in the pygmy swordtail, Xiphophorus pygmaeus.

Animal Behavior, 65, 735–743.

Kirkpatrick, M. & Ravigné, V. (2002) Speciation by natural and sexual selection: models and experiments. American Naturalist, 159, 22–35.

Kohlmann, B., Wilkinson, J. & Lulla, K. (2002) Costa Rica desde el espacio/Costa Rica from Space, 1st edn. Fundacíon Neotrópica, San José.

Lande, R. (1981) Models of speciation by sexual selection on polygenic traits. Proceedings of the National Academy of Sciences, USA, 78, 3721–3725.

Larsson, K. & Forslund, P. (1991) Environmentally induced morphological variation in the Barnacle Goose, Branta leucopsis. Journal of Evolutionary Biology, 4, 619–636.

Lee, T.J., Speed, M.P. & Stephens, P.A. (2011) Honest Signaling and the Uses of Prey Coloration. The American Naturalist , 178, 1–9.

Lemckert, F. (1996) Effects of toe-clipping on the survival and behaviour of the Australian frog Crinia signifera. Amphibia-Reptilia, 17, 287–290.

Lindstedt, C., Lindström, L. & Mappes, J. (2008) Hairiness and warning colors as components of antipredator defense: additive or interactive benefits? Animal Behaviour, 75, 1703–1713.

Lindstedt, C., Eagerb, H., Ihalainena, E., Kahilainena, A., Stevens, M. & Mappes J. (2011) Direction and strength of selection by predators for the color of the aposematic wood tiger moth. Behavioral Ecology, 22, 580–587.

Lindström, L., Alatalo, R.V. & Mappes, J. (1999a) Inherited avoidance towards color, gregariousness and conspicuousness: experiments with naive and experienced predators.

Behavioural Ecology, 10, 317–322.

Lindström, L., Alatalo, R., Mappes, J., Riipi, M. & Vertainen, L. (1999b) Can aposematic signals evolve by gradual change? Nature, 397, 249–251.

Lindström, L., Alatalo, R., Lyytinen, A. & Mappes, J. (2001a) Predator experience on cryptic prey affects the survival of conspicuous aposematic prey. Proceedings of the Royal Society of London series B, 268, 357–361.

Lindström, L., Alatalo, R.V., Lyytinen, A. & Mappes, J. (2001b) Strong antiapostatic selection against novel rare aposematic. Proceedings of the National Academy of Sciences, 98 9181–9184.

Lindström, L., Alatalo, R.V., Lyytinen, A. & Mappes, J. (2004) The effect of alternative prey on the dynamics of Batesian and Mullerian mimicries. Evolution, 58, 1294–1302.

Lougheed, S.C., Austin, J.D., Bogart, J.P., Boag, P.T. & Chek, A.A. (2006) Multi-character perspectives on the evolution of intraspecific differentiation in a neotropical hylid frog.

BMC Evolutionary Biology, 6, 23.

Lu, G. & Bernatchez, L. (1999) Correlated trophic specialization and genetic divergence in sympatric lake whitefish ecotypes (Coregonus clupeaformis) support for the ecological speciation hypothesis. Evolution, 53, 1491–1505.

Luddecke, H. (2000) Behavioral aspects of the reproductive biology of the Andean frog

Luddecke, H. (2000) Behavioral aspects of the reproductive biology of the Andean frog

Im Dokument Geographical variation in the granular poison frog, Oophaga granulifera (Seite 75-110)