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Latitude or biogeographic breaks? Determinants of phenotypic (co)variation in fitness-related traits in Betaeus truncatus along the Chilean coast

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Abstract

Ectothermal organisms distributed along environmental gradients in a wide geographical distribution display extensive phenotypic variation. This is particularly pervasive along latitudinal clines, which are linked to gradual changes in environmental factors. Widespread species may also be distributed among biogeographic breaks, which in contrast to smooth clines, often show abrupt changes in phenotypic traits. In species with widespread latitudinal distribution that also encompass important biogeographical breaks, it is not clear which of those factors prevails on shaping the phenotypic variation or if some traits are particularly more sensitive to one or the other. To evaluate this, we measured 4 fitness-related traits in 6 populations of the intertidal snapping shrimp Betaeus truncatus, as its distribution along Chile expands over 40° in latitude and three major biogeographical provinces. Here, we statistically evaluated the role of both, latitude and biogeographic breaks, on mean population values of fitness-related traits but also on the variances and covariances (i.e., P-matrix) between them. Overall, our results (1) indicate that latitude is more important than breaks in shaping the phenotypic variation of most of these fitness-related traits, (2) show that the differences in the variance–covariance relationship among traits between the extremes of the gradient arises from gradual increases in variance and rather sharp changes in covariance at mid-latitudes and (3) show that at present, it is difficult to unambiguously determine whether natural selection or plasticity is responsible for the observed pattern in means, variances and covariances and only further work might disentangle these possibilities.

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References

  • Albornoz L, Wehrtmann IS (1997) Descripción y clave de los primeros estadíos larvales de camarones carídeos (Decapoda: Hippolytidae, Alpheidae, Rhynchocinetidae) de aguas costeras de Chile. Invest Mar Valparaíso 25:121–133

    Google Scholar 

  • Arntz W, Gorny M (1996) Cruise report of the Chilean–German–Italian Magellan “Victor Hensen” Campaign in 1994. Ber Polarforsch 190:1–113

    Google Scholar 

  • Ayrinhac A, Debat V, Gibert P, Kister AG, Legout H, Moreteau B (2004) Cold adaptation in geographical populations of Drosophila melanogaster: phenotypic plasticity is more important than genetic variability. Funct Ecol 18:700–706

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B (2013). lme4: linear mixed-effects models using S4 classes. R package version 0.999999-2. http://CRAN.R-project.org/package=lme4

  • Bauer RT (1992) Testing generalization about latitudinal variation in reproduction and recruitment patterns with sicyoniid and caridean shrimp species. Invertebr Reprod Dev 22:193–202

    Article  Google Scholar 

  • Bernardo J (1996) The particular maternal effect of propagule size, especially egg size: patterns, models, quality of evidence and interpretations. Am Zool 36(2):216–236

    Google Scholar 

  • Brante A, Fernández M, Viard F (2012) Phylogeography and biogeography concordance in the marine gastropod Crepipatella dilatata (Calyptraeidae) along the southern eastern pacific coast. J Hered. doi:10.1093/jhered/ess030

    Google Scholar 

  • Camus PA (2001) Biogeografía marina de Chile continental. Rev Chil Hist Nat 74:587–617

    Article  Google Scholar 

  • Cardenas L, Castilla JC, Viard F (2009) A phylogeographic analysis across three biogeographic provinces of the southeastern Pacific: the case of the marine gastropod Concholepas concholepas. J Biogeogr 36:969–981

    Article  Google Scholar 

  • Clarke A (1987) Temperature, latitude and reproductive output. Mar Biol 38:89–99

    Google Scholar 

  • Clarke A (1992) Reproduction in the cold: Thorson revisited. Invertebr Reprod Dev 22:175–184

    Article  Google Scholar 

  • Clarke A, Hopkins CCE, Nilssen EM (1991) Egg size and reproductive output in the deepwater prawn Pandalus borealis Krøyer, 1838. Funct Ecol 5:724–730

    Article  Google Scholar 

  • Conover DO, Duffy TA, Hice LA (2009) The covariance between genetic and environmental influences across ecological gradients. Ann NY Acad Sci 1168:100–129

    Article  Google Scholar 

  • Cowen RK, Paris CB, Srinivasan A (2006) Scaling connectivity in marine populations. Science 311:522–527

    Article  CAS  Google Scholar 

  • Fox CW, Czesak ME (2000) Evolutionary ecology of progeny size in arthropods. Annu Rev Entomol 45:341–369

    Article  CAS  Google Scholar 

  • Hamilton AM, Klein ER, Austin CC (2010) Biogeographic breaks in Vanuatu, a nascent oceanic archipelago. Pac Sci 64:149–159

    Article  Google Scholar 

  • Haye PA, Varela AI, Thiel M (2012) Genetic signatures of rafting dispersal in algal-dwelling brooders Limnoria spp. (Isopoda) along the SE Pacific (Chile). Mar Ecol Prog Ser 455:111–122

    Article  Google Scholar 

  • Hoffmann AA, Sgro CM (2011) Climate change and evolutionary adaptation. Nature 470:479–485

    Article  CAS  Google Scholar 

  • Huey RB, Gilchrist GW, Carlson ML, Berrigan D, Serra L (2000) Rapid evolution of a geographic cline in size in an introduced fly. Science 287:308–309

    Article  CAS  Google Scholar 

  • Kingsolver JG, Izem R, Ragland GJ (2004) Plasticity of size and growth in fluctuating thermal environments: comparing reaction norms and performance curves. Integr Comp Biol 44:450–460

    Article  Google Scholar 

  • Krzanowski WJ (1979) Between-group comparisons of principal components. J Am Stat Assoc 74:703–707

    Google Scholar 

  • Lande R, Arnold SJ (1983) The measurement of selection on correlated characters. Evolution 36:1210–1226

    Article  Google Scholar 

  • Lardies MA, Castilla JC (2001) Latitudinal variation in the reproductive biology of commensal crab Pinnaxodes chilensis (Decapoda: Pinnotheridae) along the Chilean coast. Mar Biol 139:1125–1133

    Article  Google Scholar 

  • Lardies MA, Wehrtmann IS (1997) Egg production in Betaeus emarginatus (H. Milne Edwards, 1837) (Decapoda: Alpheidae): fecundity, reproductive output and chemical composition of eggs. Ophelia 49:165–174

    Article  Google Scholar 

  • Lardies MA, Wehrtmann IS (2001) Latitudinal variation in the reproductive biology of Betaeus truncatus (Decapoda: Alpheidae) along the Chilean coast. Ophelia 55:55–67

    Article  Google Scholar 

  • Lardies MA, Medina M, Correa J (2008) Breakage of intraspecific patterns in coastal zones associated with copper mine tailings in Chile: the snapping shrimp Betaeus emarginatus as model. Mar Ecol Prog Ser 358:203–210

    Article  Google Scholar 

  • Lardies MA, Arias MB, Bacigalupe LD (2010) Phenotypic covariance matrix in life-history traits along a latitudinal gradient: a study case in a geographically widespread crab on the coast of Chile. Mar Ecol Prog Ser 412:179–187

    Article  Google Scholar 

  • Lardies MA, Muñoz JL, Paschke KA, Bozinovic F (2011) Latitudinal variation in the aerial/aquatic ratio of oxygen consumption of a supratidal high rocky-shore crab. Mar Ecol 32:42–51

    Article  CAS  Google Scholar 

  • Macaya EC, Zuccarello GC (2010) Genetic structure of the giant kelp Macrocystis pyrifera along the southeastern Pacific. Mar Ecol Prog Ser 420:103–112

    Article  Google Scholar 

  • Meneses I, Santelices B (2000) Patterns and breaking points in the distribution of benthic algae along the temperate Pacific coast of South America. Rev Chil Hist Nat 73:615–623

    Article  Google Scholar 

  • Mitchell-Olds T, Willis JH, Goldstein DB (2007) Which evolutionary processes influence natural genetic variation for phenotypic traits? Nat Rev Genet 8:845–856

    Article  CAS  Google Scholar 

  • Mizera F, Meszéna G (2003) Spatial niche packing, character displacement and adaptive speciation along an environmental gradient. Evol Ecol Res 5:363–382

    Google Scholar 

  • Ovaskainen O, Cano JM, Merilä J (2008) A Bayesian framework for comparative quantitative genetics. Proc R Soc Lond B 275:669–678

    Article  Google Scholar 

  • Pearse JS, McClintock JB, Bosch I (1991) Reproduction of Antarctic benthic marine invertebrates: tempos, modes, and timing. Am Zool 31(1):65–80

    Google Scholar 

  • R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna Austria

    Google Scholar 

  • Ragionieri L, Fratini S, Vannini M, Schubart CD (2009) Phylogenetic and morphometric differentiation reveal geographic radiation and pseudo-cryptic speciation in a mangrove crab from the Indo-West Pacific. Mol Phylogenet Evol 52(3):825–834

    Article  CAS  Google Scholar 

  • Ricklefs RE, Wikelski M (2002) The physiology/life history nexus. Trends Ecol Evol 17:462–468

    Article  Google Scholar 

  • Rivadeneira MM, Fernandez M, Navarrete SA (2002) Latitudinal trends of species diversity in rocky intertidal herbivore assemblages: spatial-scale and the relationship between local and regional species richness. Mar Ecol Prog Ser 245:123–131

    Article  Google Scholar 

  • Robinson MR, Beckerman AP (2013) Quantifying multivariate plasticity: genetic variation in resource acquisition drives plasticity in resource allocation to components of life history. Ecol Lett 16(3):281–290

    Article  Google Scholar 

  • Roff DA, Prokkola JM, Krams I, Rantala MJ (2012) There is more than one way to skin a G matrix. J Evol Biol 25(6):1113–1126

    Article  CAS  Google Scholar 

  • Sanchez R, Sepulveda RD, Brante A, Cardenas L (2011) Spatial pattern of genetic and morphological diversity in the direct developer Acanthina monodon (Gastropoda: Mollusca). Mar Ecol Prog Ser 434:121–131

    Article  Google Scholar 

  • Sanford E, Kelly KW (2011) Local adaptation in marine invertebrates. Ann Rev Mar Sci 3:509–535

    Article  Google Scholar 

  • Sanford E, Roth MS, Johns GC, Wares JP, Somero GN (2003) Local selection and latitudinal variation in a marine predator–prey interaction. Science 300:1135–1137

    Article  CAS  Google Scholar 

  • Silva N, Rojas N, Fedele A (2009) Water masses in the Humboldt Current System: properties, distribution, and the nitrate deficit as a chemical water mass tracer for equatorial subsurface water off Chile. Deep Sea Res Part II 56:1004–1020

    Article  CAS  Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

    Google Scholar 

  • Takahashi Y, Morita S, Yoshimura J, Watanabe M (2011) A geographic cline induced by negative frequency-dependent selection. BMC Evol Biol 11:256

    Article  Google Scholar 

  • Tellier F, Meynard AP, Correa JA, Faugeron S, Valero M (2009) Phylogeographic analyses of the 30°S south–east Pacific biogeographic transition zone establish the occurrence of a sharp genetic discontinuity in the kelp Lessonia nigrescens: vicariance or parapatry? Mol Phylogenet Evol 53:679–693

    Article  CAS  Google Scholar 

  • Thiel M, Macaya E, Acuña E, Arntz W et al (2007) The Humboldt Current System of northern and central Chile: oceanographic processes, ecological interactions and socioeconomic feedback. Oceanogr Mar Biol Annu Rev 45:195–344

    Google Scholar 

  • Thorson G (1950) Reproductive and larval ecology of marine bottom invertebrates. Biol Rev 25:1–45

    Article  Google Scholar 

  • Waters JM (2008) Driven by the west wind drift? A synthesis of southern temperate marine biogeography, with new directions for dispersalism. J Biogeogr 35(3):417–427

    Article  Google Scholar 

  • Wehrtmann IS, Carvacho A (1997) New records and distribution ranges of shrimps (Crusta cea: Decapoda: Penaeoidea and Caridea) in Chilean waters. Proc Biol Soc Wash 110:49–57

    Google Scholar 

  • West BT, Welch KB, Gałecki AT, Gillespie BW (2007) Linear mixed models: a practical guide using statistical software. Chapman & Hall/CRC, Boca Raton

    Google Scholar 

  • Zakas C, Binford J, Navarette SA, Wares JP (2009) Upwelling-driven community transitions reflected in limited barnacle gene flow. Mar Ecol Prog Ser 394:165–177

    Article  Google Scholar 

Download references

Acknowledgments

Aura M. Barria acknowledges a CONICYT Doctoral Fellowship. This research was funded by FONDECYT 1110743 to Marco A. Lardies, by CONICYT MEC 800120004 to Andrew P. Beckerman and by FONDECYT 1120461 to Leonardo D. Bacigalupe. This study complies with current Chilean legislation regarding the collection and treatment of invertebrates.

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Correspondence to Leonardo D. Bacigalupe.

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Communicated by P. Kraufvelin.

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Barria, A.M., Lardies, M.A., Beckerman, A.P. et al. Latitude or biogeographic breaks? Determinants of phenotypic (co)variation in fitness-related traits in Betaeus truncatus along the Chilean coast. Mar Biol 161, 111–118 (2014). https://doi.org/10.1007/s00227-013-2319-0

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