Abstract
Iris patterns in the animal kingdom are incredibly variable, with anurans having some of the most diverse and intricate patterns. Although the shape and colouration of anuran eyes seem to be correlated with ecological factors, the evolution of iris patterns remains unexplored. We used a large-scale phylogenetic comparison with 960 anuran species to examine the evolutionary and ecological correlates of iris patterns. We classified iris patterns into four broad categories: Reticulated, Plain, Dotted, and Lined, and examined whether iris pattern was correlated with diel activity (diurnal, nocturnal, and cathemeral activity) and habit (aquatic, arboreal, terrestrial, and fossorial) or both. Our analysis suggests that reticulated irises are the most common pattern in anurans and are the most likely ancestral character. The evolution of iris patterns across the anuran phylogeny best matched Brownian expectations, with many transitions between the four pattern types. Iris patterns, however, were mostly uncorrelated with diel activity or habit. The only exception was an association between plain irises and diel activity. Specifically, anurans with plain irises were more likely to be diurnal and less likely to be nocturnal; and the evolution of plain irises seemed to have preceded the evolution of diel activity. Overall, iris patterns across anurans are mostly unrelated to ecological factors, suggesting that this trait may be important for other functions, such as inter- or intra-specific interactions, or that the incredible diversity has evolved through neutral processes. Our findings open avenues for further research, especially to understand the potential adaptive value of the striking ornamentation in iris patterns across taxonomic groups.
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References
Ackermann RR, Cheverud JM (2004) Detecting genetic drift versus selection in human evolution. Proc Natl Acad Sci U S A 101:17946–17951
Amat F, Wollenberg KC, Vences M (2013) Correlates of eye colour and pattern in mantellid frogs. Salamandra 49:7–17
AmphibiaWeb (2023) University of California, Berkeley, CA, USA. Accessed 9 Feb 2023.
Anderson SR, Wiens JJ (2017) Out of the dark: 350 million years of conservatism and evolution in diel activity patterns in vertebrates. Evolution 71:1944–1959
Baker J, Venditti C (2019) Rapid Change in mammalian Eye shape is explained by activity pattern. Curr Biol 29:1082–1088e1083
Banks MS, Sprague WW, Schmoll J, Parnell JA, Love GD (2015) Why do animal eyes have pupils of different. Shapes? Sci Adv 1:e1500391
Boyko JD, Beaulieu JM (2022) Reducing the biases in false correlations between Discrete characters. Syst Biol 72:476–488
Cervino NG, Elias-Costa AJ, Pereyra MO, Faivovich J (2021) A closer look at pupil diversity and evolution in frogs and toads. Proc Biol Sci 288:20211402
Corbett EC, Brumfield RT and B. C. Faircloth (2023) The mechanistic, genetic and evolutionary causes of bird eye colour variation. Ibis
Craig A, Hulley P (2004) Iris colour in passerine birds: why be bright-eyed? S. Afr J Sci 100:584–588
Darwin C (1859) On the origin of species by means of natural selection. J. Murray, London
Davidson GL, Thornton A, Clayton NS (2017) Evolution of iris colour in relation to cavity nesting and parental care in passerine birds. Biol Lett 13
Davis-Silberman N, Ashery-Padan R (2008) Iris development in vertebrates; genetic and molecular considerations. Brain Res 1192:17–28
Doberski J, Walmesley G (2007) Microsculpture in UK ground beetles: are there patterns? Entomol Sci 10:425–428
Douglas RH, Marshall NJ (1999) In: Archer SN, Djamgoz MBA, Loew ER, Partridge JC, Vallerga S (eds) A review of vertebrate and invertebrate ocular filters. Adaptive mechanisms in the ecology of vision Springer, pp 95–162
Duellman WE, Trueb L (1994) Biology of amphibians. Johns Hopkins University, Baltimore
Fritz SA, Purvis A (2010) Selectivity in mammalian extinction risk and threat types: a new measure of phylogenetic signal strength in binary traits. Conserv Biol 24:1042–1051
Frost DR (2024) Amphibian Species of the World: an Online Reference. Version 6.2 (4th January 2024). American Museum of Natural History, New York, USA. Electronic Database accessible at https://amphibiansoftheworld.amnh.org/index.php
Glaw F, Vences M (1997) In: Böhme W, Bischoff W, Ziegler T (eds) A review of anuran eye colouration: definitions, taxonomic implications and possible functions. Herpetologica Bonnensis. Societas Herpetologica Europaea, Bonn, Germany, pp 125–138
Grether GF, Kolluru GR, Nersissian K (2004) Individual colour patches as multicomponent signals. Biol Rev 79:583–610
Harmon L (2021) Phylogenetic comparative methods. University of Idaho, Idaho, USA
Heathcote RJP, Darden SK, Troscianko J, Lawson MRM, Brown AM, Laker PR, Naisbett-Jones LC, MacGregor HEA, Ramnarine I, Croft DP (2018) Dynamic eye colour as an honest signal of aggression. Curr Biol 28:R652–R653
Ho WC, Ohya Y, Zhang J (2017) Testing the neutral hypothesis of phenotypic evolution. Proc Natl Acad Sci U S A 114:12219–12224
Ives AR, Helmus MR (2011) Generalized linear mixed models for phylogenetic analyses of community structure. Ecol Monogr 81:511–525
Jetz W, Pyron RA (2018) The interplay of past diversification and evolutionary isolation with present imperilment across the amphibian tree of life. Nat Ecol Evol 2:850–858
Jiang Y, Chen C, Liao W (2022) Anuran interorbital distance variation: the role of ecological and behavioral factors. Integr Zool 17:777–786
Kobayashi H, Kohshima S (2001) Unique morphology of the human eye and its adaptive meaning: comparative studies on external morphology of the primate eye. J Hum Evol 40:419–435
Koch MN, Garwood RJ, Parry LA (2021) Fossils improve phylogenetic analyses of morphological characters. Proc Biol Sci 288:20210044
Land M, Nilsson DE (2002) Animal eyes. Oxford University Press, Oxford, UK
Mitra AT, Womack MC, Gower DJ, Streicher JW, Clark B, Bell RC, Schott RK, Fujita MK, Thomas KN (2022) Ocular lens morphology is influenced by ecology and metamorphosis in frogs and toads. Proc Biol Sci 289:20220767
Moazed KT (2020) Iris Anatomy. In: Moazed KT (ed) The Iris: understanding the essentials. Springer International Publishing, Cham, pp 15–29
Orme D, Freckleton R, Thomas G, Petzoldt T, Fritz S, Isaac N and W. J. R. p. v. Pearse (2012) Caper: comparative analyses of phylogenetics and evolution in R. 2:458
Pagel M (1994) Detecting correlated evolution on phylogenies: a general method for the comparative analysis fo discrete characters. Proc Royal Soc B: Biol Sci 255:37–45
Paradis E, Schliep K (2019) Ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinf (Oxf) 35:526–528
Passarotto A, Parejo D, Cruz-Miralles A, Avilés JM (2018) The evolution of iris colour in relation to nocturnality in owls. J Avian Biol 49
Perea-Garcia JO, Ramarajan K, Kret ME, Hobaiter C, Monteiro A (2022) Ecological factors are likely drivers of eye shape and colour pattern variations across anthropoid primates. Sci Rep 12:17240
Revell LJ (2012) Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223
Rowley JJ, Callaghan CT, Cornwell WKJCS, and Practice (2020) Widespread short-term persistence of frog species after the 2019–2020 bushfires in eastern Australia revealed by citizen science. 2:e287
Schmitz L, Higham TE (2018) Non-uniform evolutionary response of Gecko eye size to changes in diel activity patterns. Biol Lett 14
Schulte LM, Ringler E, Rojas B, Stynoski JL (2020) Developments in Amphibian parental Care Research: history, present advances, and future perspectives. Herpetol Monogr 34:71
Seshadri KS, Thaker M (2022) Correlated evolution of parental care with dichromatism, colours, and patterns in anurans. Evolution
Stoddard MC, Osorio D (2019) Animal coloration patterns: linking spatial vision to quantitative analysis. Am Nat 193:164–186
Thomas KN, Gower DJ, Bell RC, Fujita MK, Schott RK, Streicher JW (2020) Eye size and investment in frogs and toads correlate with adult habitat, activity pattern and breeding ecology. Proc Biol Sci 287:20201393
Thomas KN, Rich C, Quock RC, Streicher JW, Gower DJ, Schott RK, Fujita MK, Douglas RH and R. C. Bell. 2022b. Diversity and evolution of amphibian pupil shapes. Biol J Linn Soc 137:434–449
Thomas KN, Gower DJ, Streicher JW, Bell RC, Fujita MK, Schott RK, Liedtke HC, Haddad CFB, Becker CG, Cox CL, Martins RA and R. H. Douglas. 2022a. Ecology drives patterns of spectral transmission in the ocular lenses of frogs and salamanders. Funct Ecol 36:850–864
Wells KD (2007) The ecology and behavior of amphibians. Univ Chicago, Chicago, IL.
Wiens JJ, Kuczynski CA, Duellman WE, Reeder TW (2007) Loss and re-evolution of complex life cycles in marsupial frogs: does ancestral trait reconstruction mislead? Evolution 61:1886–1899
Womack MC, Steigerwald E, Blackburn DC, Cannatella DC, Catenazzi A, Che J, Koo MS, McGuire JA, Ron SR, Spencer CL, Vredenburg VT and R. D. Tarvin. 2022. State of the Amphibia 2020: A Review of Five Years of Amphibian Research and Existing Resources. Ichthyology & Herpetology 110
Yu G, Smith D, Zhu H, Guan Y, Lam T (2017) Ggtree: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol Evol 8:28–36
Zhang J (2018) Neutral theory and phenotypic evolution. Mol Biol Evol 35:1327–1331
Acknowledgements
Dr. Aparna Lajmi, Dr. Harish Prakash, and Vidisha Kulkarni provided valuable comments during the preparation of the manuscript. Chris Brown, Andrew Borcher, Esteban Alzate, John P. Clare, Brian Freiermuth, César L. Barrio Amoros, Todd Pierson, José M. Padial, Dr. Peter Janzen, and Javier Sunyer provided access to photographs. KSS was supported by the DST INSPIRE Faculty Fellowship (DST/INSPIRE/04/2019/001782) provided by the Department of Science and Technology, Govt. Of India. Comments by two anonymous reviewers further improved the quality of our MS. We thank them all.
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Seshadri was supported by the DST INSPIRE Faculty Fellowship (DST/INSPIRE/04/2019/001782) provided by the Department of Science and Technology, Govt. Of India.
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Seshadri, K.S., Gangothri, S. & Thaker, M. Does the diversity of anuran iris patterns have an ecological function or is it just beauty in the eye of the beholder?. Evol Ecol (2024). https://doi.org/10.1007/s10682-024-10293-5
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DOI: https://doi.org/10.1007/s10682-024-10293-5