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Phenotypic correlates of pelvic spine coloration in the threespine stickleback (Gasterosteus aculeatus): implications for function and evolution

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Abstract

Animal color patches may be static or plastic in expression and concealable or continuously visible, yet the evolution and function of these aspects of coloration have seldom been studied together. We investigated such color pattern elements using the threespine stickleback (Gasterosteus aculeatus). Despite a rich history of study of stickleback nuptial color pattern evolution, disagreement persists regarding selection pressures and function and only limited research has addressed the role of pelvic spine coloration, a potentially important, and substantially concealable, color pattern element. We investigated (i) whether male pelvic spine (along with throat and body) coloration is relatively static or plastic across the reproductive cycle, (ii) when pelvic spines are raised versus concealed across behavioral contexts, and (iii) associations between color patches and behavior in males. We found no significant variation in spine color across reproductive stages whereas body color was more plastic and intensely red during courtship and egg/fry care. Conspicuousness of pelvic spine coloration instead varied behaviorally, through increased erection frequency during social interactions and in response to a model predator. Spine erection frequency was positively associated with behaviors that enhance spine color visibility, i.e., flees and leads to nest. These findings suggest that stickleback use pelvic spines to display an intensely red color patch facultatively, either as a complement to similar body coloration or possibly as a substitute.

Significance statement

The interplay between color patches that are either readily concealable or always visible has been little studied, particularly in organisms with patches on a single individual that differ in capacity for concealment, such as the threespine stickleback (Gasterosteus aculeatus). While much work has been done on the evolution of coloration in stickleback, little has addressed patterns of expression and evolutionary functions of pelvic spine color, which can be facultatively concealed. We evaluated the expression characteristics of male spine coloration within the spawning period and how spine color relates to other color patches. Our work also examines the relationship between pelvic spine erections and presentation of spine color patches and raises the possibility of pelvic spine color being naturally selected and functioning across different behavioral contexts.

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Data availability

The datasets that were compiled and analyzed in this study can be accessed at the following: https://doi.org/10.5061/dryad.9kd51c5jm

References

  • Amundsen CR, Nordeide JT, Gjøen HM, Larsen B, Egeland ES (2015) Conspicuous carotenoid-based pelvic spine ornament in three-spined stickleback populations—occurrence and inheritance. PeerJ 3:e872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bakker TCM (1994) Evolution of aggressive behaviour in the threespine stickleback. In: Bell MA, Foster SA (eds) The Evolutionary Biology of the Threespine Stickleback. Oxford University Press, Oxford, pp 345–380

    Google Scholar 

  • Bakker TCM, Milinski M (1993) The advantages of being red: sexual selection in the stickleback. Mar Behav Physiol 23:287–300

    Article  Google Scholar 

  • Bakker TCM, Mundwiler B (1994) Female mate choice and male red coloration in a natural three-spined stickleback (Gasterosteus aculeatus) population. Behav Ecol 5:74–80

    Article  Google Scholar 

  • Bell MA, Foster SA (eds) (1994) The evolutionary biology of the threespine stickleback. Oxford University Press, Oxford

    Google Scholar 

  • Bigelow HB, Schroeder WC (1953) Fishes of the Gulf of Maine. US Government Printing Office, Washington

    Google Scholar 

  • Brock CD, Cummings ME, Bolnick DI (2017) Phenotypic plasticity drives a depth gradient in male conspicuousness in threespine stickleback, Gasterosteus aculeatus. Evolution 71:2022–2036

    Article  PubMed  Google Scholar 

  • Candolin U (1999) The relationship between signal quality and physical condition: is sexual signalling honest in the three-spined stickleback? Anim Behav 58:1261–1267

    Article  CAS  PubMed  Google Scholar 

  • Candolin U, Tukiainen I (2015) The sexual selection paradigm: have we overlooked other mechanisms in the evolution of male ornaments? Proc R Soc B 282:20151987

    Article  PubMed  PubMed Central  Google Scholar 

  • Clarke JM, Schluter D (2011) Colour plasticity and background matching in a threespine stickleback species pair. Biol J Linn Soc 102:902–914

    Article  Google Scholar 

  • Cuthill IC (2007) Animal behaviour: Strategic signalling by cephalopods. Curr Biol 17:R1059–R1060

    Article  CAS  PubMed  Google Scholar 

  • Cuthill IC, Allen WL, Arbuckle K, Caspers B, Chaplin G, Hauber ME, Hill GE, Jablonski NG, Jiggins CD, Kelber A (2017) The biology of color. Science 357:eaan0221

  • Duarte RC, Flores AA, Stevens M (2017) Camouflage through colour change: mechanisms, adaptive value and ecological significance. Phil Trans R Soc B 372:20160342

    Article  PubMed  PubMed Central  Google Scholar 

  • Endler JA (1984) Natural and sexual selection on color patterns in poeciliid fishes. In: Zaret TM (ed) Evolutionary ecology of neotropical freshwater fishes. Springer, Dordrecht, pp 95–111

    Chapter  Google Scholar 

  • Endler JA (1992) Signals, signal conditions, and the direction of evolution. Am Nat 139:S125–S153

    Article  Google Scholar 

  • Foster SA, Shaw KA, Robert KL, Baker JA (2008) Benthic, limnetic and oceanic threespine stickleback: profiles of reproductive behaviour. Behaviour 145:485–508

    Article  Google Scholar 

  • Friard O, Gamba M (2016) BORIS: a free, versatile open-source event-logging software for video/audio coding and live observations. Methods Ecol Evol 7:1325–1330

    Article  Google Scholar 

  • Harvey PH, Paxton RJ (1981) The evolution of aposematic coloration. Oikos 37:391–393

    Article  Google Scholar 

  • Herczeg G, Turtiainen M, Merilä J (2010) Morphological divergence of North-European nine-spined sticklebacks (Pungitius pungitius): signatures of parallel evolution. Biol J Linn Soc 101:403–416

    Article  Google Scholar 

  • Hodgson A, Black AR, Hull R (2013) Sensory exploitation and indicator models may explain red pelvic spines in the brook stickleback, Culaea inconstans. Evol Ecol Res 15:199–211

    Google Scholar 

  • Hoogland R (1951) On the fixing-mechanism in the spines of Gasterosteus aculeatus L. P K Ned Akad C Biol 54:171–180

    Google Scholar 

  • Hoogland R, Morris D, Tinbergen N (1956) The spines of sticklebacks (Gasterosteus and Pygosteus) as means of defence against predators (Perca and Esox). Behaviour 10:205–236

    Article  Google Scholar 

  • Houde AE (1987) Mate choice based upon naturally occurring color-pattern variation in a guppy population. Evolution 41:1–10

    PubMed  Google Scholar 

  • Huntingford FA (1976) The relationship between anti-predator behaviour and aggression among conspecifics in the three-spined stickleback, Gasterosteus aculeatus. Anim Behav 24:245–260

    Article  Google Scholar 

  • Johnson S, Candolin U (2017) Predation cost of a sexual signal in the threespine stickleback. Behav Ecol 28:1160–1165

    Article  Google Scholar 

  • Kim S-Y, Velando A (2014) Stickleback males increase red coloration and courtship behaviours in the presence of a competitive rival. Ethology 120:502–510

    Article  Google Scholar 

  • Kozak GM, Boughman JW (2012) Plastic responses to parents and predators lead to divergent shoaling behaviour in sticklebacks. J Evol Biol 25:759–769

    Article  PubMed  Google Scholar 

  • Kozak GM, Boughman JW (2015) Predator experience overrides learned aversion to heterospecifics in stickleback species pairs. Proc R Soc B 282:20143066

    Article  PubMed  PubMed Central  Google Scholar 

  • Kroken KK, Sæthre AA, Nicolaisen O, Egeland TB, Nordeide JT (2021) Carotenoids-based reddish pelvic spines in nonreproducing female and male sticklebacks (Gasterosteus aculeatus)–Signalling social dominance? Ecol Evol 11:11038–11050

    Article  PubMed  PubMed Central  Google Scholar 

  • Jenck CS, Lehto WR, Ketterman BT, Sloan LF, Sexton AN, Tinghitella RM (2020) Phenotypic divergence among threespine stickleback that differ in nuptial coloration. Ecol Evol 10:2900–2916

    Article  PubMed  PubMed Central  Google Scholar 

  • Loeffler-Henry K, Kang C, Yip Y, Caro T, Sherratt TN (2018) Flash behavior increases prey survival. Behav Ecol 29:528–533

    Article  Google Scholar 

  • Maia R, Gruson H, Endler JA, White TE (2019) pavo 2: new tools for the spectral and spatial analysis of colour in R. Methods Ecol Evol 10:1097–1107

    Article  Google Scholar 

  • Mazzi D, Künzler R, Bakker TCM (2003) Female preference for symmetry in computer-animated three-spined sticklebacks, Gasterosteus aculeatus. Behav Ecol Sociobiol 54:156–161

    Article  Google Scholar 

  • Mazzi D, Künzler R, Largiadèr CR, Bakker TCM (2004) Inbreeding affects female preference for symmetry in computer-animated sticklebacks. Behav Genet 34:417–424

    Article  PubMed  Google Scholar 

  • McInerney JE (1969) Reproductive behaviour of the blackspotted stickleback, Gasterosteus wheatlandi. J Fish Res Board Can 26:2061–2077

    Article  Google Scholar 

  • McKenzie JA (1969) The courtship behavior of the male brook stickleback, Culaea inconstans (Kirtland). Can J Zool 47:1281–1286

    Article  Google Scholar 

  • McKinnon JS (1995) Video mate preferences of female three-spined sticklebacks from populations with divergent male coloration. Anim Behav 50:1645–1655

    Article  Google Scholar 

  • McKinnon JS (1996) Red coloration and male parental behaviour in the threespine stickleback. J Fish Biol 49:1030–1033

    Article  Google Scholar 

  • McKinnon JS, Rundle HD (2002) Speciation in nature: the threespine stickleback model systems. Trends Ecol Evol 17:480–488

    Article  Google Scholar 

  • McKinnon JS, Demayo RF, Granquist R, Weggel L (2000) Female red throat coloration in two populations of threespine stickleback. Behaviour 137:947–963

    Article  Google Scholar 

  • McLennan DA (1996) Integrating phylogenetic and experimental analyses: the evolution of male and female nuptial coloration in the stickleback fishes (Gasterosteidae). Syst Biol 45:261–277

    Article  Google Scholar 

  • McLennan DA, McPhail JD (1989) Experimental investigations of the evolutionary significance of sexually dimorphic nuptial colouration in Gasterosteus aculeatus (L.): temporal changes in the structure of the male mosaic signal. Can J Zool 67:1767–1777

    Article  Google Scholar 

  • McLennan DA, McPhail JD (1990) Experimental investigations of the evolutionary significance of sexually dimorphic nuptial colouration in Gasterosteus aculeatus (L.): the relationship between male colour and female behaviour. Can J Zool 68:482–492

    Article  Google Scholar 

  • McLennan DA, Ward JL (2006) Changes in agonistic, courtship and parental displays of the male brook stickleback, Culaea inconstans, across the breeding cycle. Behaviour 143:33–56

    Article  Google Scholar 

  • Milinski M, Bakker TCM (1990) Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature 344:330–333

    Article  Google Scholar 

  • Moodie G (1972) Predation, natural selection and adaptation in an unusual threespine stickleback. Heredity 28:155–167

    Article  Google Scholar 

  • Morris D (1958) The reproductive behaviour of the ten-spined stickleback (Pygosteus pungitius L.). Behaviour Suppl 6:1–154

    Google Scholar 

  • Nordeide JT (2002) Do male sticklebacks prefer females with red ornamentation? Can J Zool 80:1344–1349

    Article  Google Scholar 

  • Nordeide JT, Rudolfsen G, Egeland ES (2006) Ornaments or offspring? Female sticklebacks (Gasterosteus aculeatus L.) trade off carotenoids between spines and eggs. J Evol Biol 19:431–439

    Article  CAS  PubMed  Google Scholar 

  • Ostlund-Nilsson S, Mayer I, Huntingford FA (2006) Biology of the three-spined stickleback: CRC press, Boca Raton

  • Perneger TV (1998) What’s wrong with Bonferroni adjustments. Brit Med J 316:1236–1238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reimchen T (1983) Structural relationships between spines and lateral plates in threespine stickleback (Gasterosteus aculeatus). Evolution 37:931–946

    CAS  PubMed  Google Scholar 

  • Reimchen TE (1994) Predators and morphological evolution in threespine stickleback. In: Bell MA, Foster SA (eds) The evolutionary biology of the threespine stickleback: Oxford University Press, Oxford, pp 240-276

  • Reisman HM (1963) Reproductive behavior of Apeltes quadracus, including some comparisons with other gasterosteid fishes. Copeia 1963:191–192

    Article  Google Scholar 

  • Rothman KJ (1990) No adjustments are needed for multiple comparisons. Epidemiology 1:43–46

    Article  CAS  PubMed  Google Scholar 

  • Rowland WJ (1974) Reproductive behavior of the fourspine stickleback, Apeltes quadracus. Copeia 1974:183–194

    Article  Google Scholar 

  • Rowland WJ (1982) The effects of male nuptial coloration on stickleback aggression: a reexamination. Behaviour 80:118–126

    Article  Google Scholar 

  • Rowland WJ (1984) The relationships among nuptial coloration, aggression, and courtship of male three-spined sticklebacks, Gasterosteus aculeatus. Can J Zool 62:999–1004

    Article  Google Scholar 

  • Rush V, Abney M, McKinnon JS, Sargent RC (2003) Reflectance spectra from free-swimming sticklebacks (Gasterosteus): social context and eye-jaw contrast. Behaviour 140:1003–1019

    Article  Google Scholar 

  • Scott RJ, Foster SA (2000) Field data do not support a textbook example of convergent character displacement. Proc R Soc Lond B 267:607–612

    Article  CAS  Google Scholar 

  • Smith JM, Harper D, 2003. Animal signals: Oxford University Press, Oxford

  • Stuckert AMM, Drury S, Anderson CM, Bowling TBT, Mckinnon JS (2019) Evolution and assessment of colour patterns in stream-resident and anadromous male threespine stickleback Gasterosteus aculeatus from three regions. J Fish Biol 94:520–525

    Article  PubMed  Google Scholar 

  • Symons PE (1966) Analysis of spine-raising in the male three-spined stickleback. Behaviour 26:1–75

    Article  Google Scholar 

  • Tibblin P, Hall M, Svensson PA, Merilä J, Forsman A (2020) Phenotypic flexibility in background-mediated color change in sticklebacks. Behav Ecol 31:950–959

    Article  PubMed  PubMed Central  Google Scholar 

  • Umbers KD, De Bona S, White TE, Lehtonen J, Mappes J, Endler JA (2017) Deimatism: a neglected component of antipredator defence. Biol Lett 13:20160936

    Article  PubMed  PubMed Central  Google Scholar 

  • Umbers KD, Lehtonen J, Mappes J (2015) Deimatic displays. Curr Biol 25:R58–R59

    Article  CAS  PubMed  Google Scholar 

  • van Iersel JJA (1953) An analysis of the parental behaviour of the male three-spined stickleback (Gasterosteus aculeatus L.). Behaviour Suppl 3:1–159

    Google Scholar 

  • Ward JL, McLennan DA (2006) Changes in agonistic, courtship and parental displays of the male brook stickleback, Culaea inconstans, across the breeding cycle. Behaviour 143:33–56

    Article  Google Scholar 

  • Wootton R (1971) Measures of the aggression of parental male three-spined sticklebacks. Behaviour 40:228–261

    Article  CAS  PubMed  Google Scholar 

  • Wright DS, Pierotti ME, Rundle HD, McKinnon JS (2015) Conspicuous female ornamentation and tests of male mate preference in threespine sticklebacks (Gasterosteus aculeatus). PLoS ONE 10:e0120723

    Article  PubMed  PubMed Central  Google Scholar 

  • Wright DS, Yong L, Pierotti ME, McKinnon JS (2016) Male red throat coloration, pelvic spine coloration, and courtship behaviours in threespine stickleback. Evol Ecol Res 17:407–418

    Google Scholar 

  • Yong L, Guo R, Wright DS, Mears SA, Pierotti M, McKinnon JS (2013) Correlates of red throat coloration in female stickleback and their potential evolutionary significance. Evol Ecol Res 15:453–472

    Google Scholar 

  • Yong L, Peichel CL, McKinnon JS (2016) Genetic architecture of conspicuous red ornaments in female threespine stickleback. Genes Genomes Genet 6:579–588

    Google Scholar 

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Acknowledgements

We thank the Semiahmoo First Nation for granting us permission to collect fish on their land and the British Columbia Ministry of Forests, Lands, and Natural Resource Operations for allowing fish collections within British Columbia (Permit No: MRNA17-262956 and MRSU18-290075). We thank Catherine Peichel and the Peichel Lab for guidance and use of supplies for stickleback capture. Many thanks to the East Carolina University Department of Biology and members of the McKinnon lab for help in fish care, Cole Pena and Feixiang He for assistance in color analysis, and Drew Varnell for help in edits. We are grateful to Xiangming Fang for consulting on statistical approaches and for the assistance with statistical analyses, as well as Jeffrey Cole, Lucas Tidmarsh-Cortes, Adam Stuckert, and Michael Anderson for aid with mathematical analyses and coding. Finally, thanks to Kyle Summers, Christopher Balakrishnan, and two anonymous referees for constructive feedback on earlier drafts of this manuscript.

Funding

Research reported in this publication was supported in part by the National Institute of General Medical Sciences of the National Institutes of Health under Award Number R15GM109291. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

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  1. Department of Biology, East Carolina University, Greenville, North Carolina, USA

    Christopher M. Anderson & Jeffrey S. McKinnon

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  1. Christopher M. Anderson
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CMA and JSM conceived the experiment. CMA carried out the experimental trials and data collection, CMA and JSM performed data analysis, and CMA drafted the manuscript. Both authors reviewed and edited the manuscript.

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Correspondence to Christopher M. Anderson.

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This study complied with and followed rules governed by the Institutional Animal Care and Use Committee (IACUC) at East Carolina University (Animal Use Protocol #D349). This work was possible because of approval by the British Columbia Ministry of Forests, Lands, and Natural Resource Operations for fish collection (Permit Numbers MRNA17-262956 and MRSU18-290075).

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Anderson, C.M., McKinnon, J.S. Phenotypic correlates of pelvic spine coloration in the threespine stickleback (Gasterosteus aculeatus): implications for function and evolution. Behav Ecol Sociobiol 76, 153 (2022). https://doi.org/10.1007/s00265-022-03256-9

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