Contrasting post-settlement selection results in many-to-one mapping of high performance phenotypes in the Hawaiian waterfall-climbing goby Sicyopterus stimpsoni

Abstract

Natural selection drives adaptive evolution, but contrasting environmental pressures may lead to trade-offs between phenotypes that confer different performances. Such trade-offs may weaken the strength of selection and/or generate complex fitness surfaces with multiple local optima that correspond to different selection regimes. We evaluated how differences in patterns of phenotypic selection might promote morphological differences between subpopulations of the amphidromous Hawaiian waterfall-climbing goby, Sicyopterus stimpsoni. We conducted laboratory experiments on fish from the islands of Kaua‘i and Hawai‘i (the “Big Island”) to compare patterns of linear and nonlinear selection, and the opportunity for selection, that result from two contrasting pressures, predator evasion and waterfall climbing, which vary in intensity between islands. We found directional and nonlinear selection were strongest when individuals were exposed to their primary selective pressures (predator evasion on Kaua‘i, waterfall climbing on the Big Island). However, the opportunity for selection was greater for the non-primary pressure: climbing on Kaua‘i, predator evasion on the Big Island. Canonical rotation of the nonlinear gamma matrix demonstrated that individuals from Kaua‘i and the Big Island occupy regions near their local fitness peaks for some traits. Therefore, selection for predator evasion on Kaua‘i and climbing on the Big Island may be less effective in promoting morphological changes in this species, because variation of functionally important traits in their respective environments may have been reduced by directional or stabilizing selection. These results demonstrate that despite constraints on the opportunities for selection, population differences in phenotypic traits can arise due to differences in selective regimes. For S. stimpsoni, sufficient variation exists in other locomotor traits, allowing for necessary levels of performance in the contrasting selective regime (i.e., climbing on Kaua‘i and predator evasion on the Big Island) through many-to-one-mapping, which may be essential for the survival of local populations in an evanescent island environment.

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Adapted from Moody et al. (2015)

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References

  1. Abràmoff MD, Magalhães PJ, Ram SJ (2004) Image processing with ImageJ. Biophotonics Int 11:36–42

    Google Scholar 

  2. Alfaro ME, Bolnick DI, Wainwright PC (2005) Evolutionary consequences of many-to-one mapping of jaw morphology to mechanics in labrid fishes. Am Nat 165:E140–E154

    Article  PubMed  Google Scholar 

  3. Arnold SJ (1983) Morphology, performance and fitness. Am Zool 23:347–361

    Article  Google Scholar 

  4. Arnold SJ, Wade MJ (1984) On the measurement of natural and sexual selection: applications. Evolution 38:720–734

    Article  PubMed  Google Scholar 

  5. Benkman CW (2003) Divergent selection drives the adaptive radiation of crossbills. Evolution 57:1176–1181

    Article  PubMed  Google Scholar 

  6. Ben-Tzvi O, Abelson A, Gaines SD, Bernardi G, Beldade R, Sheehy MS, Paradis GL, Kiflawi M (2012) Evidence for cohesive dispersal in the sea. PLoS ONE 7:e42672. doi:10.1371/journal.pone.0042672

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. Blob RW, Bridges WC, Ptacek MB, Maie T, Cediel RA, Bertolas MM, Julius ML, Schoenfuss HL (2008) Morphological selection in and extreme flow environment: body shape and waterfall-climbing success in the Hawaiian stream fish Sicyopterus stimpsoni. Int Comp Biol 48:734–749; (Erratum) 49:732–734 (2009)

  8. Blob RW, Kawano SM, Moody KN, Bridges WC, Maie T, Ptacek MB, Julius ML, Schoenfuss HL (2010) Morphological selection and the evaluation of potential tradeoffs between escape from predators and the climbing of waterfalls in the Hawaiian stream goby Sicyopterus stimpsoni. Int Comp Biol 50:1185–1199

    Article  Google Scholar 

  9. Blows MW (2007) A tale of two matrices: multivariate approaches in evolutionary biology. J Evol Biol 20:1–8

    CAS  Article  PubMed  Google Scholar 

  10. Blows MW, Brooks R (2003) Measuring nonlinear selection. Am Nat 162:815–820

    Article  PubMed  Google Scholar 

  11. Blows MW, Brooks R, Kraft PG (2003) Exploring complex fitness surfaces: multiple ornamentation and polymorphism in male guppies. Evolution 57:1622–1630

    Article  PubMed  Google Scholar 

  12. Brodie ED (1989) Genetic correlations between morphology and antipredator behavior in natural populations of the garter snake Thamnophis ordinoides. Nature 342:542–543

    Article  PubMed  Google Scholar 

  13. Brodie ED III (1992) Correlational selection for color pattern and antipredator behavior in the garter snake Thamnophis ordinoides. Evolution 46:1284–1298

    Article  PubMed  Google Scholar 

  14. Brodie ED III, Moore AJ, Janzen FJ (1995) Visualizing and quantifying natural selection. Trends Ecol Evol 10:313–318

    Article  PubMed  Google Scholar 

  15. Calsbeek R, Irschick DJ (2007) The quick and the dead: correlational selection on morphology, performance, and habitat use in island lizards. Evolution 61:2493–2503

    Article  PubMed  Google Scholar 

  16. Calsbeek R, Smith TB (2008) Experimentally replicated disruptive selection on performance traits in a Caribbean lizard. Evolution 62:478–484

    Article  PubMed  Google Scholar 

  17. Carlson SM, Rich HB Jr, Quinn TP (2009) Does variation in selection imposed by bears drive divergence among populations in the size and shape of sockeye salmon? Evolution 63:1244–1261

    Article  PubMed  Google Scholar 

  18. Chenoweth SF, Blows MW (2005) Contrasting mutual sexual selection on homologous signal traits in Drosophila serrata. Am Nat 165:281–289

    Article  PubMed  Google Scholar 

  19. Clague DA, Dalrymple GB (1987) Tectonics, geochronology and origin of the Hawaiian-Emperor volcanic chain. In: Decker RW, Wright TL, Stauffer PH (eds) Volcanism in Hawaii. US Geological Survey Professional Paper 1350. US Government Printing Office, Washington, DC, pp 1–54

  20. Diamond KM, Schoenfuss HL, Walker JA, Blob RW (2016) Flowing water affects fish fast-starts: escape performance of the Hawaiian stream goby, Sicyopterus stimpsoni. J Exp Biol 219:3100–3105

    Article  PubMed  Google Scholar 

  21. Doherty PJ, Dufour V, Galzin R, Hixon MA, Meekan MG, Planes S (2004) High mortality during settlement is a population bottleneck for a tropical surgeonfish. Ecology 85:242–2428

    Article  Google Scholar 

  22. Domenici P (2003) Habitat, body design, and the swimming performance of fish. In: Bels VL, Gasc J-P, Casinos A (eds) Vertebrate biomechanics and evolution. BIOS Scientific Publishers, Oxford, pp 137–160

    Google Scholar 

  23. Domenici P, Turesson H, Brodersen J, Brnmark C (2008) Predator-induced morphology enhances escape locomotion in crucian carp. Proc R Soc Lond B Biol 275:195–201

    Article  Google Scholar 

  24. Dumont ER, Samadevam K, Grosse I, Warsi OM, Baird B, Davalos LM (2014) Selection for mechanical advantage underlies multiple cranial optima in new world leaf-nosed bats. Evolution 68:1436–1449

    Article  PubMed  Google Scholar 

  25. Efron B, Gong G (1983) A leisurely look at the bootstrap, the jackknife, and cross-validation. Am Stat 37:36–48

    Google Scholar 

  26. Endler JA (1986) Natural selection in the wild. Princeton University Press, Princeton

    Google Scholar 

  27. Fields Development Team (2006) Fields: tools for spatial data. National Center for Atmospheric Research, Boulder, CO. http://www.image.ucar.edu/Software/Fields

  28. Fisher RA (1930) The genetical theory of natural selection. Oxford University Press, Oxford

    Google Scholar 

  29. Fitzsimons JM, Zink RM, Nishimoto RT (1990) Genetic variation in the Hawaiian stream goby, Lentipes concolor. Biochem Syst Ecol 18:81–83

    CAS  Article  Google Scholar 

  30. Fitzsimons JM, Nishimoto RT, Yuen AR (1993) Courtship and territorial behavior in the native Hawaiian stream goby, Sicyopterus stimpsoni. Ichthyol Explor Freshw 4:1–10

    Google Scholar 

  31. Gaines SD, Bertness MD (1992) Dispersal of juveniles and variable recruitment in sessile marine species. Nature 360:579–580

    Article  Google Scholar 

  32. Grant PR, Grant BR (2002) Unpredictable evolution in a 30-year study of Darwin’s Finches. Science 296:707–711

    CAS  Article  PubMed  Google Scholar 

  33. Hendry AP, Kinnison MT (2001) An introduction to microevolution: rate, pattern, process. Genetica 112:1–8

    Article  PubMed  Google Scholar 

  34. Hendry AP, Huber SK, De Leon LF, Herrel A, Podos J (2009) Disruptive selection in a bimodal population of Darwin’s finches. Proc R Soc Lond B Biol 276:753–759

    Article  Google Scholar 

  35. Hereford J, Hansen TF, Houle D (2004) Comparing strengths of directional selection: How strong is strong? Evolution 58:479–485

    Article  Google Scholar 

  36. Hoekstra HE, Hoekstra JM, Berriga D, Vignieri SN, Hoang A, Hill CE, Beerlii P, Kingsolver JG (2001) Strength and tempo of directional selection in the wild. Proc Natl Acad Sci USA 98:9157–9160

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  37. Hogan JD, Thiessen RJ, Heath DD (2010) Variability in connectivity indicated by chaotic genetic patchiness within and among population of a marine fish. Mar Ecol-Prog Ser 417:263–275

    Article  Google Scholar 

  38. Irschick DJ, Meyers JJ, Husak JF, Le Galliard JF (2008) How does selection operate on whole-organism functional performance capacities? A review and synthesis. Evol Ecol Res 10:177–196

    Google Scholar 

  39. Janzen FJ, Stern HS (1998) Logistic regression for empirical studies of multivariate selection. Evolution 52:1564–1571

    Article  PubMed  Google Scholar 

  40. Johannesson K, Johannesson B, Lundgren U (1995) Strong natural selection causes microscale allozyme variation in a marine snail. Proc Natl Acad Sci USA 92:2602–2606

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. Kawano SM, Bridges WC, Schoenfuss HL, Maie T, Blob RW (2013) Differences in locomotor behavior correspond to different patterns of morphological selection in two species of waterfall-climbing gobiid fishes. Evol Ecol 27:949–969

    Article  Google Scholar 

  42. Kingsolver JG, Pfennig DW (2007) Patterns and power of phenotypic selection in nature. Bioscience 57:561–572

    Article  Google Scholar 

  43. Kingsolver JG, Hoekstra HE, Hoekstra JM, Berrigan D, Vignieri SN, Hill CH, Hoang A, Gibert P, Beerli P (2001) The strength of phenotypic selection in natural populations. Am Nat 157:245–261

    CAS  Article  PubMed  Google Scholar 

  44. Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 37:1210–1226

    Article  PubMed  Google Scholar 

  45. Larson RJ, Julian RM (1999) Spatial and temporal genetic patchiness in marine populations and their implications for fisheries management. Calif Cooper Ocean Fish 40:94–99

    Google Scholar 

  46. LeBras NR, Hockham LR, Ritchie MG (2003) Nonlinear and correlational sexual selection on ‘honest’ female ornamentation. Proc R Soc Lond B Biol 270:2159–2165

    Article  Google Scholar 

  47. Lenormand T (2002) Gene flow and the limits to natural selection. Trends Ecol Evol 17:183–189

    Article  Google Scholar 

  48. Lenth RV (2009) Response-surface methods in R, using rsm. J Stat Softw 32:2–17

    Article  Google Scholar 

  49. Leonard G, Maie T, Moody KN, Schrank G, Blob RW, Schoenfuss HL (2012) Finding paradise: cues directing the migration of the waterfall climbing Hawaiian gobioid fish Sicyopterus stimpsoni. J Fish Biol 81:903–920

    CAS  Article  PubMed  Google Scholar 

  50. Losos JB (1990) The evolution of form and function: morphology and locomotor performance in West Indian Anolis lizards. Evolution 1990:1189–1203

    Article  Google Scholar 

  51. Maie T, Schoenfuss HL, Blob RW (2012) Performance and scaling of a novel locomotor structure: adhesive capacity of climbing gobiid fishes. J Exp Biol 215:3925–3936

    Article  PubMed  Google Scholar 

  52. Maie T, Schoenfuss HL, Blob RW (2013) Musculoskeletal determinants of pelvic sucker function in Hawaiian stream gobiid fishes: interspecific comparisons and allometric scaling. J Morphol 274:733–742

    Article  PubMed  Google Scholar 

  53. Maie T, Furtek S, Schoenfuss HL, Blob RW (2014) Feeding performance and functional modulation of the Hawaiian sleeper, Eleotris sandwicensis (Gobiodei: Eleotridae): implications for selection pressures on prey. Biol J Linn Soc 111:359–374

    Article  Google Scholar 

  54. Martin CH (2012) Weak disruptive selection and incomplete phenotypic divergence in two classic examples of sympatric speciation: Cameroon Crater Lake cichlids. Am Nat 180:E90–E109

    Article  PubMed  Google Scholar 

  55. Martin CH, Wainwright PC (2013) Multiple fitness peaks on the adaptive landscape drive adaptive radiation in the wild. Science 339:208–2011

    CAS  Article  PubMed  Google Scholar 

  56. McDowall RM (2003) Hawaiian biogeography and the islands’ freshwater fish fauna. J Biogeogr 30:703–710

    Article  Google Scholar 

  57. McRae MG (2007) The potential for source-sink population dynamics in Hawaii’s amphidromous fishes. Bishop Mus Bull Cult Environ Stud 3:87–98

    Google Scholar 

  58. Moody KN, Hunter SN, Childress MJ, Blob RW, Schoenfuss HL, Blum MJ, Ptacek MB (2015) Local adaptation despite high gene flow in the waterfall-climbing Hawaiian goby, Sicyopterus stimpsoni. Mol Ecol 24:545–563

    CAS  Article  PubMed  Google Scholar 

  59. Morrissey MB, Hadfield JD (2011) Directional selection in temporally replicated studies is remarkably consistent. Evolution 66:435–442

    Article  PubMed  Google Scholar 

  60. Mosimann JE, James FC (1979) New statistical methods for allometry with application to Florida red-winged blackbirds. Evolution 1979:444–459

    Article  Google Scholar 

  61. Nishimoto RT, Fitzsimons JM (1999) Behavioral determinants of the instream distribution of native Hawaiian stream fishes. In: Séret B, Sire J-Y (eds) Proceeding from the fifth Indo-Pacific fish conferences, Nouméa. Societe Francaise d’Ichthyologie, Paris, pp 813–818

    Google Scholar 

  62. Norton SF, Luczkovich JJ, Motta PJ (1995) The roles of ecomorphological studies in comparative biology of fishes. Environ Biol Fish 44:287–304

    Article  Google Scholar 

  63. Nosil P, Crespi BJ, Sandoval CP (2002) Host-plant adaptation drives the parallel evolution of reproductive isolation. Nature 417:440–443

    CAS  Article  PubMed  Google Scholar 

  64. Palumbi SR (2004) Marine reserves and ocean neighbourhoods: the spatial scale of marine populations and their management. Annu Rev Environ Resour 29:31–68

    Article  Google Scholar 

  65. Phillips PC, Arnold SJ (1989) Visualizing multivariate selection. Evolution 43:1209–1222

    Article  PubMed  Google Scholar 

  66. Pujolar JM, Maes GE, Volckaert FAM (2006) Genetic patchiness among recruits in the European eel Anguilla anguilla. Mar Ecol-Prog Ser 307:209–217

    Article  Google Scholar 

  67. Radtke RL, Kinzie RA III (1996) Evidence of a marine larval stage in endemic Hawaiian stream gobies from isolated high-elevation locations. Trans Am Fish Soc 135:613–621

    Article  Google Scholar 

  68. Radtke RL, Kinzie RA III, Shafer DJ (2001) Temporal and spatial variation in the length of larval life and size at settlement of the Hawaiian amphidromous goby Lentipes concolor. J Fish Biol 59:928–938

    Google Scholar 

  69. Reimchen TE, Nosil P (2002) Temporal variation in divergent selection on spine number in threespine stickleback. Evolution 56:2472–2483

    CAS  Article  PubMed  Google Scholar 

  70. Rundle HD, Nosil P (2005) Ecological speciation. Ecol Lett 8:336–352

    Article  Google Scholar 

  71. Sambatti JB, Rice KJ (2006) Local adaptation, patterns of selection, and gene flow in the Californian serpentine sunflower (Helianthus exilis). Evolution 60:696–710

    Article  PubMed  Google Scholar 

  72. Scharnow J, Tinnefeld K, Wegener I (2002) Fitness landscapes based on sorting and shortest paths problems. Springer, Berlin, pp 54–63

    Google Scholar 

  73. Schluter D (1995) Adaptive radiation in sticklebacks: trade-offs in feeding performance and growth. Ecology 1995:82–90

    Article  Google Scholar 

  74. Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, Oxford

    Google Scholar 

  75. Schoenfuss HL, Blob RW (2003) Kinematics of waterfall climbing in Hawaiian freshwater fishes (Gobiidae): vertical propulsion at the water-terrestrial interface. J Zool 261:191–205

    Article  Google Scholar 

  76. Schoenfuss HL, Blob RW (2007) The importance of functional morphology for fishery conservation and management: applications to Hawaiian amphidromous fishes. Bishop Mus Bull Cult Environ Stud 3:125–141

    Google Scholar 

  77. Siepielski AM, DiBattista JD, Carlso SM (2009) It’s about time: the temporal dynamics of phenotypic selection in the wild. Ecol Lett 12:1261–1276

    Article  PubMed  Google Scholar 

  78. Smith RJF, Smith J (1998) Rapid acquisition of directional preferences by migratory juveniles of two amphidromous Hawaiian gobies, Awaous guamensis and Sicyopterus stimpsoni. Environ Biol Fish 53:275–282

    Article  Google Scholar 

  79. Stinchcombe JR, Agrawal AF, Hohenlohe PA, Arnold SJ, Blows MW (2008) Estimating nonlinear selection gradients using quadratic regression coefficients: double or nothing? Evolution 62:2435–2440

    Article  PubMed  Google Scholar 

  80. Stobbe F, McPeek MA, De Block M, De Meester L, Stoks R (2009) Survival selection on escape performance and its underlying phenotypic traits: a case of many-to-one-mapping. J Evol Biol 22:1172–1182

    Article  Google Scholar 

  81. Svensson EI, Calsbeek R (2012) The adaptive landscape in evolutionary biology. Oxford University Press, Oxford

    Google Scholar 

  82. Swain DP (1992) Selective predation for vertebral phenotype in Gasterosteous aculateus: reversal in the direction of selection at different larva sizes. Evolution 46:998–1013

    PubMed  Google Scholar 

  83. Toro E, Herrel A, Irschick D (2004) The evolution of jumping performance in Caribbean Anolis lizards: solutions to biomechanical trade-offs. Am Nat 163:844–856

    Article  PubMed  Google Scholar 

  84. Van Valen L (1973) A new evolutionary law. Evol Theor 1:1–30

    Google Scholar 

  85. Wainwright PC (2015) Why are marine adaptive radiations rare in Hawai’i? Mol Ecol 24:523–524

    Article  PubMed  Google Scholar 

  86. Wainwright PC, Alfaro ME, Bolnick DI, Hulsey CD (2005) Many-to-one mapping of form to function: a general principle in organismal design? Int Comp Biol 45:256–262

    Article  Google Scholar 

  87. Walker JA (1997) Ecological morphology of lacustrine threespine stickleback Gasterosteus aculeatus (Gasterosteidae) body shape. Biol J Linn Soc 61:3–50

    Google Scholar 

  88. Walker JA (2014) The effect of unmeasured confounders on the ability to estimate a true performance or selection gradient (and other partial regression coefficients). Evolution 68:2128–2136

  89. Walter RP, Hogan JD, Blum MJ, Gagne RB, Hain EF, Gilliam JF, McIntyre PB (2012) Climate change and conservation of endemic amphidromous fishes in Hawaiian streams. Endanger Species Res 16:261–272

    Article  Google Scholar 

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Acknowledgements

We gratefully acknowledge the Hawai‘i Division of Aquatic Resources, especially Bob Nishimoto, Kim Peyton, Lance Nishiura, Wade Ishikawa, Troy Sakihara, Troy Shimoda, Tim Shindo, Darrel Kuamo’o, and Alysha Cabral for logistical support during field experiments. We thank Takashi Maie for assistance with collection and field experiments. We also thank Rose Curry and Caitlin McPherson for assistance with collecting fish morphometrics.

Funding

Primary funding was provided through National Science Foundation Grants (IOS-0817911 and IOS-0817794). Additional funding was provided by the Women’s National Farm and Garden Association Tyson Memorial Fellowship to S.K. A portion of this work was conducted while S. K. was a Postdoctoral Fellow at the National Institute for Mathematical and Biological Synthesis, an Institute sponsored by the National Science Foundation through NSF Award #DBI-1300426, with additional support from The University of Tennessee, Knoxville.

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Correspondence to Kristine N. Moody.

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K. N. Moody and S. M. Kawano shared co-first authorship.

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Moody, K.N., Kawano, S.M., Bridges, W.C. et al. Contrasting post-settlement selection results in many-to-one mapping of high performance phenotypes in the Hawaiian waterfall-climbing goby Sicyopterus stimpsoni . Evol Ecol 31, 489–516 (2017). https://doi.org/10.1007/s10682-017-9889-0

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Keywords

  • Morphology
  • Fish
  • Linear selection
  • Nonlinear selection
  • Fitness surface