Abstract
A fundamental prediction of reproductive signal evolution is that selection should favor male courtship signals that are conspicuous with respect to the surrounding media. However, many species live in heterogeneous environments where spatiotemporal variability can degrade the efficacy of signals tuned to specific conditions. One rarely considered solution to this problem is to evolve generalized signals that can effectively transmit information under most of the conditions that are likely to be encountered. Here, I present results from a study of a freshwater fish, the brook stickleback (Culaea inconstans) that are consistent with the hypothesis that sexually dimorphic body coloration has been driven by selection for conspicuousness under multiple environmental conditions. In choice tests, females showed no bias favoring a conspicuous black stimulus in simulated oligotrophic stream conditions, but showed a strong and equal bias for the black phenotype in simulated dystrophic and eutrophic streams. These data indicate that the evolution of signals that maximize achromatic contrast with the surrounding environment may be an effective mechanism for maintaining conspicuousness in heterogeneous visual environments. The repeated evolution of black color signals by stream fishes may therefore represent a specific example of this general evolutionary mechanism.
Significance statement
For active female mate choice to occur, a female must detect a male before she can choose him. Hypotheses of reproductive signal evolution based on male conspicuousness have primarily focused on the relationship between signal structure and a particular set of environmental parameters. However, many species live in environments that are variable. The results of mate-choice tests conducted in this study are consistent with the hypothesis that melanic reproductive color signaling in male brook stickleback (Culaea inconstans) has evolved to maximize the likelihood of detection and approach by females in heterogeneous environments. These results extend our understanding of signal evolution based on transmission efficacy and may explain the repeated evolution of melanic body coloration (bars, patches, and full-body coloration) in freshwater fishes.
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References
Bolnick DI, Hendrix K, Jordan A, Veen T, Brock CD (2016) Intruder colour and light environment jointly determine how nesting male stickleback respond to simulated territorial intrusions. Biol Lett 12:20160467
Boughman JW (2001) Divergent sexual selection enhances reproductive isolation in sticklebacks. Nature 411:944–948
Brock CD, Cummings M, Bolnick DI (2017) Phenotypic plasticity drives a depth gradient in male conspicuousness in threespine stickleback, Gasterosteus aculeatus. Evolution 71:2022–2036
Dawkins MS, Guilford T (1996) Sensory bias and the adaptiveness of female choice. Am Nat 148:937–942
Endler JA (1992) Signals, signal conditions, and the direction of evolution. Am Nat 139:S125–S153
Endler JA (1993) The color of light in forests and its implications. Ecol Monogr 63:1–27
Endler JA, Théry M (1996) Interacting effects of lek placement, display behavior, ambient light and color patterns in three neotropical forest-dwelling birds. Am Nat 148:421–452
Faria JJ, Dyer JRG, Clément RO, Couzin ID, Holt N, Ward AJW, Waters D, Krause J (2010) A novel method for investigating the collective behavior of fish: introducing ‘Robofish’. Behav Ecol Sociobiol 64:1211–1218
Hardin JW, Hilbe JM (2012) Generalized estimating equations, 2nd edn. Chapman & Hall/CRC, New York
Hebets EA, Elias DO, Mason AC, Miller GL, Stratton GE (2008) Substrate-dependent signaling success in the wolf spider Schizocosa retrorsa. Anim Behav 75:605–615
Heindl M, Winkler H (2003) Vertical lek placement of forest-dwelling manakin species (Aves, Pipridae) is associated with vertical gradients of ambient light. Biol J Linn Soc 80:647–658
Kodric-Brown A (1998) Sexual dichromatism and temporary color changes in the reproduction of fishes. Am Zool 38:70–82
Lythgoe JN (1979) The ecology of vision. Clarendon Press, Oxford
McDonald CG, Reimchen TE, Hawryshyn CW (1995) Nuptial color loss and signal masking in Gasterosteus: an analysis using video imaging. Behaviour 132:963–977
McLennan DA (1993) Temporal changes in the structure of the male nuptial signal in brook stickleback, Culaea inconstans (Kirtland). Can J Zool 71:1111–1119
McLennan DA (1994) Changes in female colour across the ovulatory cycle in the brook stickleback, Culaea inconstans (Kirtland). Can J Zool 72:144–153
McLennan DA (1995) Male mate choice based upon female nuptial coloration in the brook stickleback, Culaea inconstans (Kirtland). Anim Behav 50:213–221
Milner R, Jennions MD, Backwell PRY (2008) Does the environmental context of a signaling male influence his attractiveness? Anim Behav 76:1565–1570
Östlund-Nilsson S, Mayer I (2006) The biology of other sticklebacks. In: Östlund-Nilsson S, Mayer I, Huntingford FA (eds) The biology of the threespine stickleback. CRC Press, Boca Raton, pp 353–372
Pan W (2001) Akaike’s information criterion in generalized estimating equations. Biometrics 57:120–125
Paterson HEH (1985) The recognition concept of species. In: Vrbs ES (ed) Species and speciation. Transvaal Museum Monograph No. 4. Transvaal Museum, Pretoria, pp 21–29
Reimchen TE (1989) Loss of nuptial color in threespine sticklebacks (Gasterosteus aculeatus). Evolution 43:450–460
Rowland WJ (1989) Mate choice and the supernormality effect in female sticklebacks (Gasterosteus aculeatus). Behav Ecol Sociobiol 24:433–438
Ryan MJ (1990a) Sexual selection, sensory systems and sensory exploitation. In: Futuyma DJ, Antonovics J (eds) Oxford surveys in evolutionary biology, vol 7. Oxford University Press, Oxford, pp 157–195
Ryan MJ (1990b) Signals, species, and sexual selection. Am Sci 78:46–52
Schultz D, Anderson CN, Symes LB (2008) The conspicuousness of color cues in male pond damselflies depends on ambient light and visual system. Anim Behav 76:1357–1364
Scott RJ (2004) Assortative mating between adjacent populations of threespine stickleback (Gasterosteus aculeatus). Ecol Freshw Fish 13:1–7
Thery M, Pincebourde S, Feer F (2008) Dusk light environment optimizes visual perception of conspecifics in a crepuscular horned beetle. Behav Ecol 19:627–634
Tinbergen N (1951) The study of instinct. Oxford University Press, Oxford
Tinghitella RM, Lehto WR, Lierheimer VF (2018) Color and behavior differently predict competitive outcomes for divergent stickleback color morphs. Curr Zool 64:115–123
Ward JL, McLennan DA (2006) The relative influences of sexual and natural selection upon the evolution of male and female nuptial coloration in the brook stickleback, Culaea inconstans. Behaviour 143:483–510
Ward JL, McLennan DA (2009) Female mate choice based on complex visual signals in the brook stickleback, Culaea inconstans. Behav Ecol 20:1323–1333
Wilgers DJ, Hebets EA (2011) Complex courtship displays facilitate male reproductive success and plasticity in signaling across variable environments. Curr Zool 57:175–186
Wootton RJ (1976) The biology of the stickleback. Academic Press, New York
Acknowledgments
I am grateful to Deborah McLennan for discussions and resources, and Paul Venturelli for comments on an earlier version of the study. I am also grateful to three reviewers for their thoughtful comments on the manuscript.
Funding
Funding for this study was provided by an Animal Behavior Society Student Research Grant to JLW.
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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This study was carried out in strict accordance with the requirements of the Ontario’s Animals for Research Act. The University Animal Care Committee of the University of Toronto approved all protocols for research, housing, and the maintenance of fish (protocol number 20005656).
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The author declares that she has no conflict of interest.
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Communicated by J. Frommen
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Ward, J.L. Conspicuous signal evolution in heterogeneous environments. Behav Ecol Sociobiol 72, 119 (2018). https://doi.org/10.1007/s00265-018-2530-6
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DOI: https://doi.org/10.1007/s00265-018-2530-6