Abstract
Threespine stickleback exhibit a row of superficial neuromasts that project through the bony plates on each side of the trunk and which constitute an important sensory modality for detection of near-field water motion. Previously, we have shown that numbers of neuromasts on each structural plate are highly variable among populations. In the current paper, we expand this study to evaluate the extent of deviation from bilateral symmetry of 4344 fish in 57 natural and three transplant populations of threespine stickleback from lakes, streams and oceanic habitats of coastal British Columbia, predicting that neuromasts would be largely bilaterally symmetrical for optimal detection of external stimuli. In contrast, we found asymmetry in all populations, the greatest amount occurring on the anterior buttressing lateral plates and on populations with the fewest neuromasts. We found no consistent trends of signed (directional) asymmetry (SA) among the populations while relative absolute asymmetry (RAA) is lower in dystrophic (stained) habitats than in clearwater habitats (p < 0.001), except for fish with few neuromasts. Sexual dimorphism in RAA is also greater in dystrophic habitats (p < 0.001). Transplants from stained lakes to unstained ponds resulted in a 0.1% to 14% difference in RAA from the source population in less than 12 generations but varied in direction among experiments. Our data suggest a widespread tendency for populations exposed to reduced photic information to exhibit reduced asymmetry in their lateral line system, which can change rapidly in response to a new environment.
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References
Ahnelt H, Ramler D, Madsen MØ et al (2021) Diversity and sexual dimorphism in the head lateral line system in North Sea populations of threespine sticklebacks, Gasterosteus aculeatus (Teleostei: Gasterosteidae). Zoomorphology 140:103–117
Almeida D, Almodóvar A, Nicola GG, Elvira B (2008) Fluctuating asymmetry, abnormalities and parasitism as indicators of environmental stress in cultured stocks of goldfish and carp. Aquaculture 279:120–125
Anfora G, Rigosi E, Frasnelli E et al (2011) Lateralization in the invertebrate brain: left-right asymmetry of olfaction in bumble bee Bombus Terrestris. PLoS ONE 6:e18903
Baker CF, Montgomery JC (1999) The sensory basis of rheotaxis in the blind Mexican cave fish, Astyanax fasciatus. J Comp Physiol A 184:519–527
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Beasley DAE, Bonisoli-Alquati A, Mousseau TA (2013) The use of fluctuating asymmetry as a measure of environmentally induced developmental instability: a meta-analysis. Ecol Ind 30:218–226
Bergstrom CA, Reimchen TE (2000) Functional implications of fluctuating asymmetry among endemic populations of Gasterosteus aculeatus. Behaviour 137:1097–1112
Bergstrom CA, Reimchen TE (2005) Habitat dependent associations between parasitism and fluctuating asymmetry among endemic stickleback populations. J Evol Biol 18:939–948
Bleckmann H, Tittel G, Blübaum-Gronau E (1989) The lateral line system of surface-feeding fish: anatomy, physiology, and behavior. In: Coombs S, Görner P, Münz H (eds) The Mechanosensory Lateral Line. Springer, New York, NY, pp 501–526
Brown EEA, Simmons AM (2016) Variability of rheotaxis behaviors in larval bullfrogs highlights species diversity in lateral line function. PLoS ONE 11:e0166989
Burt de Perera T, Braithwaite VA (2005) Laterality in a non-visual sensory modality—the lateral line of fish. Curr Biol 15:R241–R242
Butler JM, Maruska KP (2016) Mechanosensory signaling as a potential mode of communication during social interactions in fishes. J Exp Biol 219:2781–2789
Cantalupo C, Bisazza A, Vallortigara G (1995) Lateralization of predator-evasion response in a teleost fish (Girardinus falcatus). Neuropsychologia 33:1637–1646
Cnaan A, Laird NM, Slasor P (1997) Using the general linear mixed model to analyse unbalanced repeated measures and longitudinal data. Stat Med 16:2349–2380
Coombs S, Patton P (2009) Lateral line stimulation patterns and prey orienting behavior in the Lake Michigan mottled sculpin (Cottus bairdi). J Comp Physiol A 195:279
Coombs S, Bleckmann H, Fay RR, Popper AN (eds) (2014) The lateral line system. Springer-Verlag, New York
Deagle BE, Jones FC, Chan YF et al (2012) Population genomics of parallel phenotypic evolution in stickleback across stream–lake ecological transitions. Proc R Soc B-Biol Sci 279:1277–1286
Engqvist L (2005) The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies. Anim Behav 70:967–971
Faucher K, Fichet D, Miramand P, Lagardère JP (2006) Impact of acute cadmium exposure on the trunk lateral line neuromasts and consequences on the “C-start” response behaviour of the sea bass (Dicentrarchus labrax L.; Teleostei, Moronidae). Aquat Toxicol 76:278–294
Fernandes VFL, Macaspac C, Lu L, Yoshizawa M (2018) Evolution of the developmental plasticity and a coupling between left mechanosensory neuromasts and an adaptive foraging behavior. Dev Biol 441:262–271
Fischer EK, Soares D, Archer KR et al (2013) Genetically and environmentally mediated divergence in lateral line morphology in the Trinidadian guppy (Poecilia reticulata). J Exp Biol 216:3132–3142
Frasnelli E, Vallortigara G, Rogers LJ (2012) Left–right asymmetries of behaviour and nervous system in invertebrates. Neurosci Biobehav R 36:1273–1291
Greenwood AK, Wark AR, Yoshida K, Peichel CL (2013) Genetic and neural modularity underlie the evolution of schooling behavior in threespine sticklebacks. Curr Biol 23:1884–1888
Gross JB, Gangidine A, Powers AK (2016) Asymmetric facial bone fragmentation mirrors asymmetric distribution of cranial neuromasts in blind Mexican cavefish. Symmetry-Basel 8:118
Harrison XA, Donaldson L, Correa-Cano ME et al (2018) A brief introduction to mixed effects modelling and multi-model inference in ecology. PeerJ 6:e4794
Hart NS, Partridge JC, Cuthill IC (2000) Retinal asymmetry in birds. Curr Biol 10:115–117
Holzman R, Perkol-Finkel S, Zilman G (2014) Mexican blind cavefish use mouth suction to detect obstacles. J Exp Biol 217:1955–1962
Houle D (1997) A meta-analysis of the heritability of developmental stability - Comment. J Evol Biol 10:17–20
Jiang Y, Peichel CL, Torrance L et al (2017) Sensory trait variation contributes to biased dispersal of threespine stickleback in flowing water. J Evol Biol 30:681–695
Junges CM, Lajmanovich RC, Peltzer PM et al (2010) Predator-prey interactions between Synbranchus marmoratus (Teleostei: Synbranchidae) and Hypsiboas pulchellus tadpoles (Amphibia: Hylidae): Importance of lateral line in nocturnal predation and effects of fenitrothion exposure. Chemosphere 81:1233–1238
Kelley JL, Grierson PF, Davies PM, Collin SP (2017) Water flows shape lateral line morphology in an arid zone freshwater fish. Evol Ecol Res 18:411–428
Krings M, Mueller-Limberger E, Wagner H (2019) EvoDevo in owl ear asymmetry-The little owl (Athene noctua). Zoology 132:1–5
Lajus DL, Golovin PV, Yurtseva AO et al (2019) Fluctuating asymmetry as an indicator of stress and fitness in stickleback: a review of the literature and examination of cranial structures. Evol Ecol Res 20:83–106
Leaver S (2010) Morphological and behavioural responses of threespine stickleback (Gasterosteus aculeatus) to abrupt alterations in their selective landscape. University of Victoria
Leaver SD, Reimchen TE (2012) Abrupt changes in defence and trophic morphology of the giant threespine stickleback (Gasterosteus sp.) following colonization of a vacant habitat. Biol J Lin Soc 107:494–509
Lens L, Dongen SV, Kark S, Matthysen E (2002) Fluctuating asymmetry as an indicator of fitness: can we bridge the gap between studies? Biol Rev 77:27–38
Lenth R (2019) emmeans: estimated marginal means, aka least-squares means
Leung B, Forbes MR, Houle D (2000) Fluctuating asymmetry as a bioindicator of stress: comparing efficacy of analyses involving multiple traits. Am Nat 155:101–115
Liao JC (2006) The role of the lateral line and vision on body kinematics and hydrodynamic preference of rainbow trout in turbulent flow. J Exp Biol 209:4077–4090
Lin L-Y, Hung G-Y, Yeh Y-H et al (2019) Acidified water impairs the lateral line system of zebrafish embryos. Aqua Toxicol 105351
Lippolis G, Joss JMP, Rogers LJ (2009) Australian Lungfish (Neoceratodus forsteri): a missing link in the evolution of complementary side biases for predator avoidance and prey capture. Brain Behav Evolut 73:295–303
Lychakov DV, Rebane YT, Lombarte A et al (2006) Fish otolith asymmetry: morphometry and modeling. Hearing Res 219:1–11
Lychakov DV, Rebane YT, Lombarte A et al (2008) Saccular otolith mass asymmetry in adult flatfishes. J Fish Biol 72:2579–2594
Markow TA, Clarke GM (1997) Meta-analysis of the heritability of developmental stability: a giant step backward. J Evol Biol 10:31–37
Marques DA, Jones FC, Di Palma F et al (2018) Experimental evidence for rapid genomic adaptation to a new niche in an adaptive radiation. Nat Ecol Evol 2:1128-+
Mekdara PJ, Schwalbe MAB, Coughlin LL, Tytell ED (2018) The effects of lateral line ablation and regeneration in schooling giant danios. J Exp Bio 221:jeb175166
Mesa MG, Warren JJ (1997) Predator avoidance ability of juvenile chinook salmon (Oncorhynchus tshawytscha) subjected to sublethal exposures of gas-supersaturated water. Can J Fish Aquat Sci 54:757–764
Middlemiss KL, Cook DG, Jerrett AR, Davison W (2017) Morphology and hydro-sensory role of superficial neuromasts in schooling behaviour of yellow-eyed mullet (Aldrichetta forsteri). J Comp Physiol A 203:807–817
Mills MG, Greenwood AK, Peichel CL (2014) Pleiotropic effects of a single gene on skeletal development and sensory system patterning in sticklebacks. EvoDevo 5:5
Mogdans J (2019) Sensory ecology of the fish lateral-line system: Morphological and physiological adaptations for the perception of hydrodynamic stimuli. J Fish Biol 95:53–72
Moller AP (1997) Developmental stability and fitness: a review. Am Nat 149:916–932
Møller AP, Thornhill R (1997) A meta-analysis of the heritability of developmental stability. J Evol Biol 10:1–16
Montgomery JC (1989) Lateral line detection of planktonic prey. In: Coombs S, Görner P, Münz H (eds) The mechanosensory lateral line. Springer, New York, NY, pp 561–574
Montgomery JC, Baker CF, Carton AG (1997) The lateral line can mediate rheotaxis in fish. Nature 389:960–963
Moodie GEE (1972) Predation, natural selection and adaptation in an unusual threespine stickleback. Heredity 28:155–167
Moodie GEE, Moodie PF (1996) Do asymmetric sticklebacks make better fathers? Proc R Soc B-Biol Sci 263:535–539
Moodie GEE, Reimchen TE (1976) Phenetic variation and habitat differences in Gasterosteus populations of the Queen Charlotte Islands. Syst Biol 25:49–61
Murtaugh PA (2009) Performance of several variable-selection methods applied to real ecological data. Ecol Lett 12:1061–1068
Niemeier S, Müller J, Rödel M-O (2019) Fluctuating asymmetry-appearances are deceptive. Comparison of methods for assessing developmental instability in European Common Frogs (Rana temporaria). Salamandra 55:14–26
Oravec TJ, Reimchen TE (2013) Divergent reproductive life histories in Haida Gwaii stickleback (Gasterosteus spp.). Can J Zool 91:17–24
Palmer AR, Strobeck C (1986) Fluctuating asymmetry: measurement, analysis, patterns. Annu Rev Ecol Syst 17:391–421
Planidin NP, Reimchen TE (2019) Spatial, sexual, and rapid temporal differentiation in neuromast expression on lateral plates of Haida Gwaii threespine stickleback (Gasterosteus aculeatus). Can J Zool 97:988–996
Pomiankowski A (1997) Genetic variation in fluctuating asymmetry. J Evol Biol 10:51–55
R Core Team (2020) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria
Reimchen TE (1989) Loss of nuptial color in threespine sticklebacks (Gasterosteus aculeatus). Evolution 43:450–460
Reimchen TE (1990) Size-structured mortality in a threespine stickleback (Gastrosteus aculeatus)—cutthroat trout (Oncorhynchus clarki) community. Can J Fish Aquat Sci 47:1194–1205
Reimchen TE, Bergstrom CA (2009) The ecology of asymmetry in stickleback defense structures. Evolution 63:115–126
Reimchen TE, Nosil P (2001) Lateral plate asymmetry, diet and parasitism in threespine stickleback. J Evol Biol 14:632–645
Reimchen TE, Nosil P (2004) Variable predation regimes predict the evolution of sexual dimorphism in a population of threespine stickleback. Evolution 58:1274–1281
Reimchen TE, Nosil P (2006) Replicated ecological landscapes and the evolution of morphological diversity among Gasterosteus populations from an archipelago on the west coast of Canada. Can J Zool 84:643–654
Reimchen TE, Ingram T, Hansen SC (2008) Assessing niche differences of sex, armour and asymmetry phenotypes using stable isotope analyses in Haida Gwaii sticklebacks. Behaviour 145:561–577
Reimchen TE, Bergstrom CA, Nosil P (2013) Natural selection and the adaptive radiation of Haida Gwaii stickleback. Evol Ecol Res 15:241–269
Reimchen TE, Steeves D, Bergstrom CA (2016) Sex matters for defence and trophic traits of threespine stickleback. Evol Ecol Res 17:459–485
Rogers LJ (2017) A matter of degree: strength of brain asymmetry and behaviour. Symmetry 9:57
Schmitz A, Bleckmann H, Mogdans J (2014) The lateral line receptor array of cyprinids from different habitats. J Morphol 275:357–370
Schwalbe MAB, Bassett DK, Webb JF (2012) Feeding in the dark: lateral-line-mediated prey detection in the peacock cichlid Aulonocara stuartgranti. J Exp Biol 215:2060–2071
Spoljaric MA, Reimchen TE (2007) 10 000 years later: evolution of body shape in Haida Gwaii three-spined stickleback. J Fish Biol 70:1484–1503
Suli A, Watson GM, Rubel EW, Raible DW (2012) Rheotaxis in larval zebrafish Is mediated by lateral line mechanosensory hair cells. PLoS ONE 7:e29727
Trokovic N, Herczeg G, McCairns SRJ et al (2011) Intraspecific divergence in the lateral line system in the nine-spined stickleback (Pungitius pungitius): Lateral line variation in sticklebacks. J Evol Biol 24:1546–1558
Trokovic N, Herczeg G, Ab Ghani NI et al (2012) High levels of fluctuating asymmetry in isolated stickleback populations. BMC Evol Biol 12:115
Wada H, Ghysen A, Satou C et al (2010) Dermal morphogenesis controls lateral line patterning during postembryonic development of teleost fish. Dev Biol 340:583–594
Wark AR, Peichel CL (2010) Lateral line diversity among ecologically divergent threespine stickleback populations. J Exp Biol 213:108–117
Wark AR, Mills MG, Dang L-H et al (2012) Genetic architecture of variation in the lateral line sensory system of threespine sticklebacks. G3-Genes Genom Genet 2:1047–1056
Werner YL, Seifan T (2006) Eye size in geckos: asymmetry, allometry, sexual dimorphism, and behavioral correlates. J Morphol 267:1486–1500
Westin L (1998) The spawning migration of European silver eel (Anguilla anguilla L.) with particular reference to stocked eel in the Baltic. Fish Res 38:257–270
York CA, Bartol IK (2014) Lateral line analogue aids vision in successful predator evasion for the brief squid, Lolliguncula brevis. J Exp Biol 217:2437–2439
Yoshizawa M, Robinson BG, Duboué ER et al (2015) Distinct genetic architecture underlies the emergence of sleep loss and prey-seeking behavior in the Mexican cavefish. BMC Biol 13:15
Zucchini W (2000) An introduction to model selection. J Math Psychol 44:41–61
Acknowledgements
We thank S. Douglas, C. Bergstrom, and M. Spoljaric for field assistance and R. Marx, J. Taylor, and D. Wertman for discussion on this manuscript.
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Financial support was provided by a King-Platt Fellowship to NP Planidin and a Natural Sciences and Engineering Council of Canada (NSERC) operating grant to TE Reimchen (NRC2354).
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Sample and biophysical data collection and research design was conducted by TE Reimchen. Lab work and data analysis was conducted by NP Planidin as part of a Master of Science. The manuscript was first drafted by NP Planidin and revised with the assistance of TE Reimchen.
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Planidin, N.P., Reimchen, T.E. Ecological predictors of lateral line asymmetry in stickleback (Gasterosteus aculeatus). Evol Ecol 35, 609–629 (2021). https://doi.org/10.1007/s10682-021-10117-w
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DOI: https://doi.org/10.1007/s10682-021-10117-w