Body size and allometric shape variation in the molly Poecilia vivipara along a gradient of salinity and predation

BMC Evolutionary Biology

Ana C Petry¹  Maria Julia C Magazoni²  S Ivan Perez³  Márcio S Araújo² 

[1] Núcleo em Ecologia e Desenvolvimento Socioambiental de Macaé – NUPEM, Universidade Federal do Rio de Janeiro – UFRJ, Macaé, RJ, Brazil;Departamento de Ecologia, Universidade Estadual Paulista, Rio Claro, SP, Brazil;División Antropología, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, CONICET, La Plata, Argentina

关键词: Poeciliidae;    Morphometrics;    Hoplias malabaricus;    Ecological gradients;    Divergent natural selection;   

Others  :  1121779
DOI  :  10.1186/s12862-014-0251-7

 received in 2014-10-21, accepted in 2014-11-20,  发布年份 2014

【 摘 要 】

Background

Phenotypic diversity among populations may result from divergent natural selection acting directly on traits or via correlated responses to changes in other traits. One of the most frequent patterns of correlated response is the proportional change in the dimensions of anatomical traits associated with changes in growth or absolute size, known as allometry. Livebearing fishes subject to predation gradients have been shown to repeatedly evolve larger caudal peduncles and smaller cranial regions under high predation regimes. Poecilia vivipara is a livebearing fish commonly found in coastal lagoons in the north of the state of Rio de Janeiro, Brazil. Similar to what is observed in other predation gradients, lagoons inhabited by P. vivipara vary in the presence of piscivorous fishes; contrary to other poeciliid systems, populations of P. vivipara vary greatly in body size, which opens the possibility of strong allometric effects on shape variation. Here we investigated body shape diversification among six populations of P. vivipara along a predation gradient and its relationship with allometric trajectories within and among populations.

Results

We found substantial body size variation and correlated shape changes among populations. Multivariate regression analysis showed that size variation among populations accounted for 66% of shape variation in females and 38% in males, suggesting that size is the most important dimension underlying shape variation among populations of P. vivipara in this system. Changes in the relative sizes of the caudal peduncle and cranial regions were only partly in line with predictions from divergent natural selection associated with predation regime.

Conclusions

Our results suggest the possibility that adaptive shape variation among populations has been partly constrained by allometry in P. vivipara. Processes governing body size changes are therefore important in the diversification of this species. We conclude that in species characterized by substantial among-population differences in body size, ignoring allometric effects when investigating divergent natural selection’s role in phenotypic diversification might not be warranted.

【 授权许可】

   
2014 Araújo et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Barton NH, Briggs DE, Eisen JA, Goldstein DB, Patel NH: Evolution. 1st edition. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY; 2007.
• [2]Endler JA: Geographic Variation, Speciation, and Clines. Princeton University Press, Princeton, NJ; 1977.
• [3]Schluter D: The Ecology of Adaptive Radiation. Oxford University Press, Inc., New York; 2000.
• [4]Schluter D: Evidence for Ecological Speciation and Its Alternative. Science 2009, 323(5915):737-741.
• [5]Carroll SP, Hendry AP, Reznick DN, Fox CW: Evolution on ecological time-scales. Funct Ecol 2007, 21:387-393.
• [6]Reznick DN, Shaw FH, Rodd FH, Shaw RG: Evaluation of the rate of evolution in natural populations of guppies (Poecilia reticulata). Science 1997, 275(5308):1934-1937.
• [7]Lande R: Quantitative genetic analysis of multivariate evolution, applied to brain: body size allometry. Evolution 1979, 31(1):402-416.
• [8]Cheverud JM: Phenotypic, genetic, and environmental morphological integration in the cranium. Evolution 1982, 36(3):499-516.
• [9]Cheverud JM: Developmental integration and the evolution of pleiotropy. Am Zool 1996, 36(1):44-50.
• [10]Shingleton AW, Frankino WA, Flatt T, Nijhout HF, Emlen DJ: Size and shape: the developmental regulation of static allometry in insects. BioEssays 2007, 29(6):536-548.
• [11]Schluter D: Adaptive radiation along genetic lines of least resistance. Evolution 1996, 50(5):1766-1774.
• [12]Klingenberg C: There’s something afoot in the evolution of ontogenies. BMC Evol Biol 2010, 10(1):221. BioMed Central Full Text
• [13]Klingenberg C: Heterochrony and allometry: the analysis of evolutionary change in ontogeny. Biol Rev 1998, 73(1):79-123.
• [14]Marroig G, Cheverud JM: A comparison of phenotypic variation and covariation patterns and the role of phylogeny, ecology, and ontogeny during cranial evolution of New World monkeys. Evolution 2001, 55(12):2576-2600.
• [15]Drake AG, Klingenberg CP: The pace of morphological change: historical transformation of skull shape in St Bernard dogs. Proc R Soc B Biol Sci 2008, 275(1630):71-76.
• [16]Mitteroecker P, Gunz P, Bernhard M, Schaefer K, Bookstein FL: Comparison of cranial ontogenetic trajectories among great apes and humans. J Hum Evol 2004, 46(6):679-698.
• [17]Gonzalez PN, Perez SI, Bernal V: Ontogenetic allometry and cranial shape diversification among human populations from South America. Anat Rec Adv Integr Anat Evol Biol 2011, 294(11):1864-1874.
• [18]Langerhans RB: Predicting evolution with generalized models of divergent selection: a case study with poeciliid fish. Integr Comp Biol 2010, 50(6):1167-1184.
• [19]Endler JA: Multiple-trait coevolution and environmental gradients in guppies. Trends Ecol Evol 1995, 10(1):22-29.
• [20]Reznick DN, Ghalambor CK, Crooks K: Experimental studies of evolution in guppies: a model for understanding the evolutionary consequences of predator removal in natural communities. Mol Ecol 2008, 17(1):97-107.
• [21]Langerhans RB: Trade-off between steady and unsteady swimming underlies predator-driven divergence in Gambusia affinis. J Evol Biol 2009, 22(5):1057-1075.
• [22]Langerhans RB: Morphology, performance, fitness: functional insight into a post-Pleistocene radiation of mosquitofish. Biol Lett 2009, 5(4):488-491.
• [23]Langerhans RB, Gifford ME, Joseph EO: Ecological speciation in Gambusia fishes. Evolution 2007, 61(9):2056-2074.
• [24]Langerhans RB, Layman CA, Shokrollahi AM, DeWitt TJ: Predator-driven phenotypic diversification in Gambusia affinis. Evolution 2004, 58(10):2305-2318.
• [25]Langerhans RB, Makowicz AM: Shared and unique features of morphological differentiation between predator regimes in Gambusia caymanensis. J Evol Biol 2009, 22(11):2231-2242.
• [26]Lucinda P: Family Poeciliidae. In Check List of the Freshwater Fishes of South and Central America. Edited by Reis RE, Kullander SO, Ferraris CJ Jr. Edipucrs, Porto Alegre; 2003:555-581.
• [27]Di Dario F, Petry AC, Pereira MMS, Mincarone MM, Agostinho LS, Camara EM, Caramaschi EP, Britto MR: An update on the fish composition (Teleostei) of the coastal lagoons of the Restinga de Jurubatiba national park and the Imboassica lagoon, northern Rio de Janeiro state. Acta Limnologica Brasiliensia 2013, 25(3):257-278.
• [28]Caliman A, Carneiro LS, Santangelo JM, Guariento RD, Pires APF, Suhett AL, Quesado LB, Scofield V, Fonte ES, Lopes PM, Sanches LF, Azevedo FD, Marinho CC, Bozelli RL, Esteves FA, Farjalla VF: Temporal coherence among tropical coastal lagoons: a search for patterns and mechanisms. Braz J Biol 2010, 70(3):803-814.
• [29]Caramaschi EP, Sanchez-Botero JI, Hollanda-Carvalho P, Brandão CAS, Soares CL, Novaes JLC, Bartolette R: Peixes das Lagoas Costeiras do Norte Fluminense: Estudos de Caso. In Pesquisas de Longa Duração na Restinga de Jurubatiba: Ecologia, História Natural e Conservação. Edited by Rocha CFD, Esteves FA, Scarano FR. RiMa, São Carlos, SP; 2004:309-337.
• [30]Gomes JL Jr, Monteiro LR: Morphological divergence patterns among populations of Poecilia vivipara (Teleostei Poeciliidae): test of an ecomorphological paradigm. Biol J Linn Soc Lond 2008, 93:799-812.
• [31]Monteiro LR, Gomes JL Jr: Morphological divergence rate tests for natural selection: uncertainty of parameter estimation and robustness of results. Genet Mol Biol 2005, 28(2):345-355.
• [32]Neves FM, Monteiro LR: Body shape and size divergence among populations of Poecilia vivipara in coastal lagoons of south-eastern Brazil. J Fish Biol 2003, 63(4):928-941.
• [33]Klingenberg C: Evolution and development of shape: integrating quantitative approaches. Nat Rev Genet 2010, 11(9):623-635.
• [34]INMET - Instituto Nacional de Meteorologia: Estação Campos. Brasil: Ministério da Agricultura, Pecuária e Abastecimento. http://www.inmet.gov.br.
• [35]Mitteroecker P, Gunz P: Advances in geometric morphometrics. Evol Biol 2009, 36(2):235-247.
• [36]Rohlf FJ: TpsDig2. 2008. available at http://life.bio.sunysb.edu/morph.
• [37]Peres-Neto P, Jackson D: How well do multivariate data sets match? The advantages of a Procrustean superimposition approach over the Mantel test. Oecologia 2001, 129(2):169-178.
• [38]Rohlf FJ, Slice DE: Extensions of the procrustes method for the optimal superimposition of landmarks. Syst Zool 1990, 39:40-59.
• [39]Mitteroecker P, Bookstein F: Linear discrimination, ordination, and the visualization of selection gradients in modern morphometrics. Evol Biol 2011, 38(1):100-114.
• [40]Rohlf FJ: Relative warp analysis and an example of its application to mosquito wings. Contributions Morphometrics 1993, 8:131-159.
• [41]Albrecht GH: Multivariate analysis and the study of form, with special reference to canonical variate analysis. Am Zool 1980, 20(4):679-693.
• [42]Klingenberg CP: MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour 2011, 11(2):353-357.
• [43]Sheets HD, Covino KM, Panasiewicz JM, Morris SR: Comparison of geometric morphometric outline methods in the discrimination of age-related differences in feather shape. Front Zool 2006, 3(1):1-12. BioMed Central Full Text
• [44]Mitteroecker P, Gunz P, Bookstein FL: Heterochrony and geometric morphometrics: a comparison of cranial growth in Pan paniscus versus Pan troglodytes. Evol Dev 2005, 7(3):244-258.
• [45]Blackith RE, Reyment RA: Multivariate Morphometrics. Academic Press, London; 1971.
• [46]Klingenberg CP, Marugán-Lobón J: Evolutionary covariation in geometric morphometric data: analyzing integration, modularity, and allometry in a phylogenetic context. Syst Biol 2013, 62(4):591-610.
• [47]R Development Core Team: R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria; 2014.
• [48]Trexler JC, Travis J: Phenotypic plasticity in the sailfin molly, Poecilia latipinna (Pisces: Poeciliidae). I. Field experiments. Evolution 1990, 44(1):143-156.
• [49]Martin SB, Hitch AT, Purcell KM, Klerks PL, Leberg PL: Life history variation along a salinity gradient in coastal marshes. Aquat Biol 2009, 8(1):15-28.
• [50]Araújo LG, Monteiro LR: Growth pattern and survival in populations of Poecilia vivipara (Teleostei; Poeciliidae) inhabiting an environmental gradient: a common garden study. Environ Biol Fish 2013, 96(8):941-951.
• [51]Shikano T, Fujio Y: Strain differences in seawater adaptability in newborn guppy Poecilia reticulata. Fish Sci 1998, 64(6):987-988.
• [52]Purcell KM, Hitch AT, Klerks PL, Leberg PL: Adaptation as a potential response to sea-level rise: a genetic basis for salinity tolerance in populations of a coastal marsh fish. Evol Appl 2008, 1(1):155-160.
• [53]Langerhans RB: Evolutionary consequences of predation: avoidance, escape, reproduction, and diversification. In Predation in Organisms: A Distinct Phenomenon. Edited by Elewa AMT. Springer-Verlag, Heidelberg; 2006:177-220.
• [54]Vd A, Hahn N, Vazzoler AM: Feeding patterns in five predatory fishes of the high Paraná River floodplain (PR, Brazil). Ecol Freshw Fish 1997, 6(3):123-133.
• [55]de los Angeles Bistoni M, Haro JG, Gutiérrez M: Feeding of Hoplias malabaricus in the wetlands of Dulce river (Córdoba, Argentina). Hydrobiologia 1995, 316(2):103-107.
• [56]Stearns SC: The Evolution of Life Histories, vol. 249. Oxford University Press, Oxford; 1992.
• [57]Tobler M, DeWitt TJ, Schlupp I, de León FJ G, Herrmann R, Feulner PG, Tiedemann R, Plath M: Toxic hydrogen sulfide and dark caves: phenotypic and genetic divergence across two abiotic environmental gradients in Poecilia mexicana. Evolution 2008, 62(10):2643-2659.
• [58]Langerhans RB, Reznick DN: Ecology and evolution of swimming performance in fishes: predicting evolution with biomechanics. In Fish Locomotion: An Etho-ecological Perspective. Edited by Domenici P, Kapoor BG. Science Publishers, Enfield; 2009:200-248.
• [59]Heinen J, Coco M, Marcuard M, White D, Peterson MN, Martin R, Langerhans RB: Environmental drivers of demographics, habitat use, and behavior during a post-Pleistocene radiation of Bahamas mosquitofish (Gambusia hubbsi). Evol Ecol 2013, 27(5):971-991.
• [60]Reznick D, Bryant M: Comparative long-term mark-recapture studies of guppies (Poecilia reticulata): differences among high and low predation localities in growth and survival. Ann Zool Fenn 2007, 44:152-160.
• [61]Johnson JB, Zúñiga-Vega JJ: Differential mortality drives life-history evolution and population dynamics in the fish Brachyrhaphis rhabdophora. Ecology 2009, 90(8):2243-2252.
• [62]Petry AC, Gomes LC, Piana PA, Agostinho AA: The role of the predatory trahira (Pisces: Erythrinidae) in structuring fish assemblages in lakes of a Neotropical floodplain. Hydrobiologia 2010, 651:115-126.
• [63]Mazzeo N, Iglesias C, Teixeira-de Mello F, Borthagaray A, Fosalba C, Ballabio R, Larrea D, Vilches J, Garcia S, Pacheco JP, Jeppesen E: Trophic cascade effects of Hoplias malabaricus (Characiformes, Erythrinidae) in subtropical lakes food webs: a mesocosm approach. Hydrobiologia 2010, 644(1):325-335.
• [64]Langerhans RB, DeWitt TJ: Shared and unique features of evolutionary diversification. Am Nat 2004, 164(3):335-349.
• [65]Marroig G, Cheverud J: Size as a line of least evolutionary resistance: diet and adaptive morphological radiation in New World monkeys. Evolution 2005, 59:1128-1142.
• [66]Berner D, Stutz WE, Bolnick DI: Foraging trait (co)variances in stickleback evolve deterministically and do not predict trajectories of adaptive diversification. Evolution 2010, 64(8):2265-2277.
• [67]Martin L, Suguio K, Dominguez JML, Flexor JM: Geologia do quaternário costeiro do litoral Norte do Rio de Janeiro e do Espírito Santo. Belo Horizonte, CPRM; 1997.
• [68]Araújo MS, Perez SI, Magazoni MJC, Petry AC: Data from: Body size and allometric shape variation in the molly Poecilia vivipara along a gradient of salinity and predation.Dryad Digital Repository. http://dx.doi.org/10.5061/dryad.4h31p.