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Investigating the role of body size, ecology, and behavior in anuran eye size evolution

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Abstract

Vertebrate eye size typically scales hypoallemetrically with body size—as animals grow larger their eyes get relatively smaller. Additionally, eye size is highly variable across species, and such variability often reflects functional adaptations to differences in behavior and/or ecology. The selective pressures underlying the evolution of eye size are especially well studied in birds, mammals, and fishes. However, whether similar scaling rules and selective pressures also underlie the evolution of eye size in amphibians remains enigmatic. Variation in eye size is intimately linked with variation in brain anatomy, as the retina is ontogenetically part of the brain. Eye size may therefore coevolve with brain size. Here we use phylogenetic comparative methods to study interspecific variation in eye volume across 44 species of anurans from 8 families from the Hengduan Mountains, China. We relate this variation to key factors known to impact eye size evolution in other vertebrate taxa such as body mass, habitat use, defense strategy and foraging mobility. We found that also in anurans eyes size scaled hypoallometrically with body mass. However, neither of the behavioral or ecological factors explained any variation in relative eye size in our sample. Whether this is representative for other frog species needs to be clarified. We therefore conclude that eye size in frogs is tightly linked to body mass evolution but that, at least in the species investigated here, none of our tested ecological and behavioral factors have a strong influence on eye size evolution.

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References

  • Blumstein DT, Fernández-Juricic E, LeDee O, Larsen E, Rodriguez-Prieto I, Zugmeyer C (2004) Avian risk assessment: effects of perching height and detectability. Ethology 110:273–285

    Article  Google Scholar 

  • Brooke MD, Hanley S, Laughlin SB (1999) The scaling of eye size with body mass in birds. Proc R Soc B 266:405–412

    Article  PubMed Central  Google Scholar 

  • Cai YL, Mai CL, Yu X, Liao WB (2018) Effect of population density on relationship between pre- and postcopulatory sexual traits. Anim Biol. https://doi.org/10.1163/15707563-20181057

    Article  Google Scholar 

  • Caves E, Sutton TT, Johnsen S (2017) Visual acuity in ray-finned fishes correlates with eye size and habitat. J Exp Biol 220:1586–1596

    Article  PubMed  Google Scholar 

  • Caves EM, Brandley NC, Johnsen S (2018) Visual acuity and the evolution of signals. Trends Ecol Evol 33:358–372

    Article  PubMed  Google Scholar 

  • Collett TS (1977) Stereopsis in toads. Nature 267:349–351

    Article  CAS  PubMed  Google Scholar 

  • Corral-López A, Garate-Olaizola M, Buechel SD, Kolm N, Kotrschal A (2017) On the role of body size, brain size, and eye size in visual acuity. Behav Ecol Sociobiol 71:179

    Article  PubMed  PubMed Central  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Busserolles F, Fitzpatrick JL, Paxton JR (2013) Eye-size variability in deep-sea lanternfishes (Myctophidae): an ecological and phylogenetic study. PLoS ONE 8:e58519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Busserolles F, Fitzpatrick JL, Marshall NJ, Collin SP (2014) The influence of photoreceptor size and distribution on optical sensitivity in the eyes of lanternfishes (Myctophidae). PLoS ONE 9:e99957

    Article  PubMed  PubMed Central  Google Scholar 

  • Dobberfuhl AP, Ullmann JFP, Shumway CA (2005) Visual acuity, environmental complexity, and social organization in African cichlid fishes. Behav Neurosci 119:1648–1655

    Article  PubMed  Google Scholar 

  • Douglas RH, Hawryshyn CW (1990) Behavioral studies of fish vision: an analysis of visual capabilities. In: Douglas RH, Djamgoz MBA (eds) The visual system of fish. Chapman and Hall, London, pp 373–418

    Chapter  Google Scholar 

  • Dreher CE, Cummings ME, Pröhl H (2015) An analysis of predator selection to affect Aposematic coloration in a poison frog species. PLoS ONE 10(6):e0130571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ewert JP, Burghagen H, Schürg-Pfeiffer E (1983) Neuroethological analysis of the innate releasing mechanism for prey-catching behaviour in toads. In: Ewert JP, Burghagen H, Schürg-Pfeiffer E (eds) Advances in vertebrate neuroethology. Plenum Press, New York, pp 413–475

    Chapter  Google Scholar 

  • Fei L, Ye CY, Jiang JP (2010) Colored Atlas of China Amphibians. Sichuan Publishing House of Science and Technology, Chengdu

    Google Scholar 

  • Freckleton RP, Harvey PH, Page M (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160:712–726

    Article  CAS  PubMed  Google Scholar 

  • Garamszegi LZ, Møller AP, Erritzøe J (2002) Coevolving avian eye size and brain size in relation to prey capture and nocturnality. Proc R Soc B 269:961–967

    Article  PubMed  PubMed Central  Google Scholar 

  • Gu J, Li DY, Luo Y, Ying SB, Zhang LY, Shi QM, Chen J, Zhang SP, Zhou ZM, Liao WB (2017) Brain size in Hylarana guentheri seems unaffected by variation in temperature and growth season. Anim Biol 67:209–225

    Article  Google Scholar 

  • Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw 33:1–22

    Article  Google Scholar 

  • Hall MI, Ross CF (2007) Eye shape and activity pattern in birds. J Zool 271:437–444

    Article  Google Scholar 

  • Harvey PH, Krebs JR (1990) Comparing brains. Science 249:140–146

    Article  CAS  PubMed  Google Scholar 

  • Huber R, Rylander MK (1992) Brain morphology and turbidity preference in Notropis and related genera (Cyprinidae, Teleostei). Environ Biol Fish 33:153–165

    Article  Google Scholar 

  • Huber R, van Staaden M, Kaufman LS, Liem KF (1997) Microhabitat use, trophic patterns and the evolution of brain structure in African cichlids. Brain Behav Evol 50:167–182

    Article  CAS  PubMed  Google Scholar 

  • Husband S, Shimizu T (2001) Evolution of the avian visual system. In: Cook RG (ed) Avian visual cognition. Tufts University E-book, Medford

    Google Scholar 

  • Iglesias TL, Dornburg A, Warren DL, Wainwright PC, Schmitz L, Economo EP (2018) Eyes Wide Shut: the impact of dim-light vision on neural investment in marine teleosts. J Evol Biol 31:1082–1092

    Article  PubMed  Google Scholar 

  • Ingle D (1976) Behavioral correlates of central visual function in anurans. In: Llinás R, Precht W (eds) Frog neurobiology. Springer, Berlin, pp 435–451

    Chapter  Google Scholar 

  • Iwaniuk A (2016) Functional correlates of brain and brain region sizes in nonmammalian vertebrates. In: Kaas JH (ed) Evolution of nervous systems. Academic Press, London, pp 335–348

    Google Scholar 

  • Jerison HJ (1973) Evolution of the brain and intelligence. Academic Press, New York

    Google Scholar 

  • Jiang A, Zhong MJ, Xie M, Lou SL, Jin L, Jehle R, Liao WB (2015) Seasonality and age is positively related to brain size in Andrew’s toad (Bufo andrewsi). Evol Biol 42:339–348

    Article  Google Scholar 

  • Kilmer JT, Rodríguez RL (2017) Ordinary least squares regression is indicated for studies of allometry. J Evol Biol 30:4–12

    Article  CAS  PubMed  Google Scholar 

  • Kiltie RA (2000) Scaling of visual acuity with body size in mammals and birds. Funct Ecol 14:226–234

    Article  Google Scholar 

  • Kotrschal K, Van Staaden MJ, Huber R (1998) Fish brains: evolution and environmental relationships. Rev Fish Biol Fisher 8:373–408

    Article  Google Scholar 

  • Kotrschal A, Buechel S, Zala S, Corral-Lopez A, Penn DJ, Kolm N (2015) Brain size affects female but not male survival under predation threat. Ecol Lett 18:646–652

    Article  PubMed  PubMed Central  Google Scholar 

  • Land MF, Nilsson DE (2012) Animal eyes. Oxford University Press, Oxford

    Book  Google Scholar 

  • Liao WB, Lou SL, Zeng Y, Merilä J (2015a) Evolution of anuran brains: disentangling ecological and phylogenetic sources of variation. J Evol Biol 28:1986–1996

    Article  CAS  PubMed  Google Scholar 

  • Liao WB, Liu WC, Merilä J (2015b) Andrew meets Rensch: sexual size dimorphism and the inverse of Rensch’s rule in Andrew’s toad (Bufo andrewsi). Oecologia 177:389–399

    Article  PubMed  Google Scholar 

  • Liao WB, Lou SL, Zeng Y, Kotrschal A (2016a) Large brains, small guts: the expensive tissue hypothesis supported in anurans. Am Nat 188:693–700

    Article  PubMed  Google Scholar 

  • Liao WB, Luo Y, Lou SL, Jehle R (2016b) Geographic variation in life-history traits: growth season affects age structure, egg size and clutch size in Andrew’s toad (Bufo andrewsi). Front Zool 13:6

    Article  PubMed  PubMed Central  Google Scholar 

  • Liao WB, Huang Y, Zeng Y, Zhong MJ, Lüpold S (2018) Ejaculate evolution in external fertilizers: Influenced by sperm competition or sperm limitation? Evolution 72:4–17

    Article  CAS  PubMed  Google Scholar 

  • Lisney TJ, Collin SP (2007) Relative eye size in elasmobranchs. Brain Behav Evol 69:266–279

    Article  PubMed  Google Scholar 

  • Liu YT, Luo Y, Gu J, Jiang S, Li DY, Liao WB (2018) The relationship between brain size and digestive tract length do not support expensive-tissue hypothesis in Hylarana guentheri. Acta Herpetol 13:141–146

    CAS  Google Scholar 

  • MacIver MA, Schmitz L, Mugan U, Murphey TD, Mobley DC (2017) Massive increase in visual range preceded the origin of terrestrial vertebrates. Proc Natl Acad Sci USA 114:E2375–E2384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mai CL, Liao WB (2019) Brain size evolution in anurans: a review. Anim Biol. https://doi.org/10.1163/15707563-00001074

    Article  Google Scholar 

  • Mai CL, Liao J, Zhao L, Liu SM, Liao WB (2017) Brain size evolution in the frog Fejervarya limnocharis supports neither the cognitive buffer nor the expensive brain hypothesis. J Zool 302:63–72

    Article  Google Scholar 

  • Martin GR (1982) An owl’s eye: schematic optics and visual performance in Strix aluco L. J Comp Physiol 145:341–349

    Article  Google Scholar 

  • Martin GR (1985) Eye. In: King AS, McClelland J (eds) Form and function in birds, vol 3. Academic Press, London, pp 311–373

    Google Scholar 

  • Martin GR (1993) Producing the image. In: Zeigler HP, Bischof HJ (eds) Vision brain, and behavior in birds. MIT Press, Cambridge, pp 5–24

    Google Scholar 

  • Martin GR (2007) Visual fields and their functions in birds. J Ornithol 148:S547–S562

    Article  Google Scholar 

  • Martins EP, Hansen TF (1997) Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. Am Nat 149:646–667

    Article  Google Scholar 

  • Møller AP, Erritzøe J (2010) Flight distance and eye size in birds. Ethology 116:458–465

    Article  Google Scholar 

  • Nilsson DE, Warrant EJ, Johnsen S, Hanlon R, Shashar N (2012) A unique advantage for giant eyes in giant squid. Curr Biol 22:683–688

    Article  CAS  PubMed  Google Scholar 

  • Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290

    Article  CAS  PubMed  Google Scholar 

  • R Development Core Team (2015) R: a language and environment for statistical computing. R Development Core Team, Vienna

    Google Scholar 

  • Rambaut A, Drummond A (2014) Tracer v1.6. https://tree.bio.ed.ac.uk/software/tracer/

  • Revell LJ (2012) Phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223

    Article  Google Scholar 

  • Rohlf FJ (2004) TpsDig 1.40. Department of Ecology and Evolution, State University at Stony Brook, New York

    Google Scholar 

  • Ross CF, Hall MI, Heesy CP (2006) Were basal primates nocturnal? evidence from eye and orbit shape. In: Ravosa M, Dagosto M (eds) Primate origins and adaptations. Kluwer, New York, pp 233–256

    Google Scholar 

  • Schmitz L, Wainwright PC (2011) Nocturnality constrains morphological and functional diversity in the eyes of reef fishes. BMC Evol Biol 11:338

    Article  PubMed  PubMed Central  Google Scholar 

  • Starunov VV, Voronezhskaya EE, Nezlin LP (2017) Development of the nervous system in Platynereis dumerilii (Nereididae, Annelida). Front Zool 14:27. https://doi.org/10.1186/s12983-017-0211-3

    Article  PubMed  PubMed Central  Google Scholar 

  • Striedter GF (2005) Principles of brain evolution. Sinauer Associates, Sunderland

    Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang T, Luo Y, Huang CH, LiaoWB HW (2018) Variation in somatic condition and testes mass in Feirana quadranus along an altitudinal gradient. Anim Biol 68:277–288

    Article  Google Scholar 

  • Veilleux CC, Kirk EC (2014) Visual acuity in mammals: effect of eye size and ecology. Brain Behav Evol 83:43–53

    Article  PubMed  Google Scholar 

  • Walls GL (1942) The vertebrate eye and its adaptive radiation. Cranbrook Institute of Science, Bloomfield Hills

    Google Scholar 

  • Warrant E (2000) The eyes of deep-sea fishes and the changing nature of visual scenes with depth. Philos Trans R Soc B 355:1155–1159

    Article  CAS  Google Scholar 

  • Warrant EJ, Locket NA (2004) Vision in the deep sea. Biol Rev 79:671–712

    Article  PubMed  Google Scholar 

  • Wells KD (2007) The ecology and behaviour of amphibians. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Werner YL, Broza M (1969) Hypothetical function of elevated locomotory postures in geckos (Reptilia: Gekkonidae). Isr J Zool 18:349–355

    Google Scholar 

  • Werner C, Himstedt W (1984) Eye accommodation during prey capture behavior in salamanders (Salamandra salamandra). Behav Brain Res 12:69–73

    Article  CAS  PubMed  Google Scholar 

  • Wu QG, Lou SL, Zeng Y, Liao WB (2016) Spawning location promotes evolution of bulbus olfactorius size in anurans. Herpetol J 26:247–250

    Google Scholar 

  • Wylie DR, Gutiérrez-Ibáñez C, Iwaniukm AN (2015) Integrating brain, behavior and phylogeny to understand the evolution of sensory systems in birds. Front Neurosci 9:281

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang SN, Feng H, Jin L, Zhou ZM, Liao WB (2018) No evidence for the expensive-tissue hypothesis in Fejervarya limnocharis. Anim Biol 68:265–276

    Article  Google Scholar 

  • Yopak KE, Lisney TJ (2012) Allometric scaling of the optic tectum in cartilaginous fishes. Brain Behav Evol 80:108–126

    Article  PubMed  Google Scholar 

  • Yu X, Zhong MJ, Li DY, Jin L, Liao WB, Kotrschal A (2018) Large-brained frogs mature later and live longer. Evolution 72:1174–1183

    Article  PubMed  Google Scholar 

  • Zeng Y, Lou SL, Liao WB, Jehle R (2014) Evolution of sperm morphology in anurans: insights into the roles of mating system and spawning location. BMC Evol Biol 14:104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zeng Y, Lou SL, Liao WB, Jehle R, Kotrschal A (2016) Sexual selection impacts brain anatomy in frogs and toads. Ecol Evol 6:7070–7079

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhong MJ, Yu X, Liao WB (2018) A review for life-history traits variation in frogs especially for anurans in China. Asian Herpetol Res 9:165–174

    Google Scholar 

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Acknowledgements

We thank Long Jin, Yi Luo, Jian Ping Yu, Min Xie and Ao Jiang help with the fieldwork and the lab work. Financial support was provided by the National Natural Sciences Foundation of China (31772451 to W.B.L.), the Key Cultivation Foundation of China West Normal University (17A006 to W.B.L.) and Talent Project of China West Normal University (17YC335 to W.B.L.), the Science and Technology Youth Innovation Team of Sichuan Province (19CXTD0022 to W.B.L.), and Vetenskapsrådet (2017-04957 to A.K.) and Swedish Research Council (2017-04957 to A.K.). All the methods used in this study related to capture and handling of the animals comply with the guidelines recommended by the Institutional Animal Care and Use Committee (IACUC) in China West Normal University. We receive permission to collect samples from all Nature Reserves of the Hengduan Mountains. We declare that all animals used in the study are treated humanely and ethically following all applicable institutional animal care guidelines in China. The field studies do not involve endangered or protected species.

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  1. Chun Hua Huang and Mao Jun Zhong contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of Southwest China Wildlife Resources Conservation (Ministry of Education), China West Normal University, Nanchong, 637009, Sichuan, China

    Chun Hua Huang, Mao Jun Zhong & Wen Bo Liao

  2. Key Laboratory of Artificial Propagation and Utilization in Anurans of Nanchong City, China West Normal University, Nanchong, 637009, Sichuan, China

    Chun Hua Huang, Mao Jun Zhong & Wen Bo Liao

  3. Institute of Eco-Adaptation in Amphibians and Reptiles, China West Normal University, Nanchong, 637009, Sichuan, China

    Chun Hua Huang, Mao Jun Zhong & Wen Bo Liao

  4. Zoological Institute, Stockholm University, 10691, Stockholm, Sweden

    Alexander Kotrschal

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  1. Chun Hua Huang
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Correspondence to Wen Bo Liao.

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Huang, C.H., Zhong, M.J., Liao, W.B. et al. Investigating the role of body size, ecology, and behavior in anuran eye size evolution. Evol Ecol 33, 585–598 (2019). https://doi.org/10.1007/s10682-019-09993-0

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