Abstract
Lutzomyia cruciata (Diptera: Phlebotominae) is an important Leishmania vector with wide distribution in America. However, geographical patterns of morphological variation of populations along its longitudinal and latitudinal distribution are still unknown. In this work, we quantified morphological variation and disparity in 243 specimens (females) from nine sample groups of Lu. cruciata from two biogeographical provinces in Mexico: Veracruzan Province (five groups) and Yucatan Peninsula Province (four groups). We registered two linear morphometric data of a reproductive structure (spermatheca) and one landmark configuration for wing shape. Our questions were if intraspecific morphological variation and disparity are related to contrasting environmental factors in these two provinces. First, our results from canonical variates analyses of the spermatheca and wing shape revealed more differences among groups of specimens within a biogeographic province than between. Second, our regression analyses revealed that morphometric variation is weakly related to 20 environmental variables considered for the two biogeographic provinces. Levels of morphological disparity in the spermatheca and wing shape within the two provinces are the same regardless of environmental homogeneity in the Yucatan Province or heterogeneity in the Veracruzan Province. These patterns of morphological variation and disparity weakly correlated with environmental variables suggest that intraspecific variation in Lu. cruciata is not clinal within a province. Subsequent investigations will be required to elucidate suspected correlations of local discontinuous phenotypes with genetic divergence within a biogeographical province.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00435-019-00450-8/MediaObjects/435_2019_450_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00435-019-00450-8/MediaObjects/435_2019_450_Fig2_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00435-019-00450-8/MediaObjects/435_2019_450_Fig3_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00435-019-00450-8/MediaObjects/435_2019_450_Fig4_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00435-019-00450-8/MediaObjects/435_2019_450_Fig5_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs00435-019-00450-8/MediaObjects/435_2019_450_Fig6_HTML.png)
Similar content being viewed by others
References
Arrivillaga J, Mutebi JP, Pinango H, Norris D, Alexander B, Feliciangeli MD, Lanzaro GC (2003) The taxonomic status of genetically divergent populations of Lutzomyia longipalpis (Diptera: Psychodidae) based on the distribution of mitochondrial and isozyme variation. J Med Entomol 40(5):615–627. https://doi.org/10.1603/0022-2585-40.5.615
Atkinson D (1994) Temperature and organism size: a biological law for ectotherms? Adv Ecol Res 25(3):1–58
Aytekin AM, Alten B, Caglar SS, Ozbel Y, Kaynas S, Simsek FM, Kasap OE, Belen A (2007) Phenotypic variation among local populations of phlebotomine sand flies (Diptera: Psychodidae) in southern Turkey. J Vector Ecol 32(2):226–234. https://doi.org/10.3376/1081-1710(2007)32%5b226:PVALPO%5d2.0.CO;2
Azevedo CR, Lainson R, Souza AA, Nelson F, Feliciangeli MD, Meneses C, Rangel E (2002) Comparative studies of populations of Lutzomyia umbratilis (Diptera: Psychodidae) in Brazil and Venezuela. J Med Entomol 39(4):587–600. https://doi.org/10.1603/0022-2585-39.4.587
Azpurua J, De La Cruz D, Valderama A, Windsor D (2010) Lutzomyia sand fly diversity and rates of infection by Wolbachia and an exotic Leishmania species on Barro Colorado Island, Panama. PLoS Negl Trop Dis 4(3):e627. https://doi.org/10.1371/journal.pntd.0000627
Belen A, Alten B (2006) Variation in life table characteristics among populations of Phlebotomus papatasi at different altitudes. J Vector Ecol 31(1):35–44. https://doi.org/10.3376/1081-1710(2006)31%5b35:VILTCA%5d2.0.CO;2
Biagi F, de Biagi AM, Beltrán F (1966) Actividad horaria de Phlebotomus antropofílicos en la Península de Yucatán. Rev Inv Salud Publica (México) 26:73–77
Birdsdall K, Zimmerman E, Teeteret K, Gibson G (2000) Genetic variation for the positioning of wing in Drosophila melanogaster. Evol Dev 2:16–24. https://doi.org/10.1046/j.1525-142x.2000.00034.x
Bordbar A, Soleimani S, Fardid F, Zolfaghari MR, Parvizi P (2014) Three strains of Wolbachia pipientis and high rates of infection in Iranian sandfly species. Bull Entomol Res 104(2):195–202. https://doi.org/10.1017/S0007485313000631
Brisola-Marcondes C (2007) A proposal of generic and subgeneric abbreviations for phlebotominae sandflies (Diptera: Psychodidae: Phlebotominae) of the world. Entomol News 118(4):351–356. https://doi.org/10.3157/0013-872X(2007)118%5b351:APOGAS%5d2.0.CO;2
Brisola-Marcondes C, Leuch-Lozovei A, Falqueto A, Brazil AP, Galati EAB, Aguilar GM, Souza NA (1999) Influence of altitude, latitude and season of collection (Bergmann’s Rule) on the dimension of Lutzomyia intermedia (Luz & Neiva, 1919) (Diptera, Psychodidae, Phlebotominae). Mem Inst Oswaldo Cruz 94(5):693–700
Cruz-Ruiz AL, García-Rejón J, Manrique-Saide P, Pérez-Mutul J (1994) Taxonomical identification of anthropophilic species of Lutzomyia in Quintana Roo, Peninsula of Yucatan. Mexico. Rev Biomed. 5:127–131
Cuervo-Robayo AP, Téllez-Valdés O, Gómez-Albores MA, Venegas-Barrera CS, Manjarrez J, Martínez-Meyer E (2013) An update of high-resolution monthly climate surfaces for Mexico. Int J Climatol. https://doi.org/10.1002/joc.3848
Cui L, Chang SH, Strickman D, Rowton E (1999) Frequency of Wolbachia infection in laboratory and field sand fly (Diptera: Psychodidae) populations. J Am Mosq Control Assoc 15(4):571–572
De la Riva J, Le Pont F, Ali V, Matias A, Mollinedo S, Dujardin JP (2001) Wing geometry as tool for studying the Lutzomyia longipalpis (Diptera: Psychodidae) complex. Mem Inst Oswaldo Cruz 96(8):1089–1096. https://doi.org/10.1590/S0074-02762001000800011
De Souza Freitas MT, Ríos-Velásquez C, Costa CR, Figueirêdo CA, Aragão NC, da Silva LG, de Aragão Batista MV, Balbino TC, Pessoa FA, de Queiroz Balbino V (2015) Phenotypic and genotypic variations among three allopatric populations of Lutzomyia umbratilis, main vector of Leishmania guyanensis. Parasit Vectors 8(1):448. https://doi.org/10.1186/s13071-015-1051-7
Dujardin JP, Pont Le (2004) Geographic variation of metric properties within neotropical sandflies. Infect Genet Evol 4(4):353–359. https://doi.org/10.1016/j.meegid.2004.05.001
Dujardin JP, Torrez EM, Le Pont F, Hervas D, Sossa D (1997) Isozymic and metric variation in the Lutzomyia longipalpis complex. Med Vet Entomol 11(4):394–400. https://doi.org/10.1111/j.1365-2915.1997.tb00428.x
Dujardin JP, Le Pont F, Martinez E (1999) Quantitative morphological evidence for incipient species within Lutzomyia quinquefer (Diptera: Psychodidae). Mem Inst Oswaldo Cruz 94(6):829–836. https://doi.org/10.1590/S0074-02761999000600022
Florin AD, Rebollar-Téllez EA (2013) Divergence of Lutzomyia (Psathyromyia) shannoni (Diptera: Psychodidae: Phlebotominae) is indicated by morphometric and molecular analyses when examined between taxa from the southeastern United States and Southern Mexico. J Med Entomol 50(6):1324–1329. https://doi.org/10.1603/ME13085
Galati EAB (2003) Classificação de Phlebotominae e morfologia, terminologia de adultos e identificação dos táxons da América. In: Rangel EF, Laison R (eds) Flebotomíneos do Brasil. Fiocruz, Rio de Janeiro, pp 23–51
Giordani BF, Andrade AJ, Galati EAB, Gurgel-Goncalves R (2017) The role of wing geometric morphometrics in the identification of sandflies within the subgenus Lutzomyia. Med Vet Entomol 31(4):373–380. https://doi.org/10.1111/mve.12245
González C, Rebollar-Téllez EA, Ibáñez-Bernal S, Becker-Fauser I, Martínez-Meyer E, Peterson T, Sánchez-Cordero V (2011) Current knowledge of Leishmania vectors in Mexico: how geographic distributions of species relate to transmission areas. Am J Trop Med Hyg 85(5):839–846. https://doi.org/10.4269/ajtmh.2011.10-0452
Guillerme T (2018) dispRity: a modular R package for measuring disparity. Methods Ecol Evol 00:1–9. https://doi.org/10.1111/2041-210X.13022
Ibáñez-Bernal, S. (2000) Los Phlebotominae (Diptera: Psychodidae) de México. Tesis de Doctorado. Universidad Nacional Autónoma de México
Ibáñez-Bernal S (2005a) Phlebotominae (Diptera: Psychodidae) de México. V. Clave ilustrada para la identificación de los machos de Lutzomyia França. Folia Entomol Mex 44(2):49–66
Ibáñez-Bernal S (2005b) Phlebotominae (Diptera: Psychodidae) de México. VI. Clave ilustrada para la identificación de las hembras de Lutzomyia França. Folia Entomol Mex 44(2):195–212
Killick-Kendrick R (1990) Phlebotomine vectors of the leishmaniasis, a review. Med Vet Entomol 4(1):1–24. https://doi.org/10.1111/j.1365-2915.1990.tb00255.x
Lorenz C, Almeida F, Almeida-Lopes F, Louise C, Pereira SN, Petersen V, Vidal VO, Virginio F, Suesdek L (2017) Geometric morphometrics in mosquitoes: what has been measured? Infect Genet Evol 54:205–215. https://doi.org/10.1016/j.meegid.2017.06.029
Marcondes CB, Lozovei AL, Falqueto A, Brazil RP, Galati E, Aguiar G, Souza N (1999) Influence of altitude, latitude and season of collection (Bergmann’s rule) on the dimensions of Lutzomyia intermedia (Lutz & Neiva, 1912) (Diptera, Psychodidae, Phlebotominae). Mem Inst Oswaldo Cruz 94(5):693–700. https://doi.org/10.1590/S0074-02761999000500026
Margonari CS, Fortes-Dias CL, Dias ES (2004) Genetic variability in geographical populations of Lutzomyia whitmani elucidated by RAPD-PCR. J Med Entomol 41(2):187–192. https://doi.org/10.1603/0022-2585-41.2.187
Marshall JL (2007) Rapid evolution of spermathecal duct length in the Allonemobius socius complex of crickets: species population and wolbachia effects. PLoS One 2:e720. https://doi.org/10.1371/journal.pone.0000720
Méndez-Pérez C, Rebollar-Téllez EA (2012) Análisis morfométrico de poblaciones alopátricas de Lutzomyia olmeca olmeca y Lutzomyia cruciata (Diptera: Psychodidae: Phlebotominae), vectores principales de la leishmaniasis cutánea en el sureste de México. Biomedica 23:7–21. https://doi.org/10.32776/revbiomed.v23i1.91
Mikery-Pacheco O, Marina-Fernández C, Ibáñez-Bernal S, Sánchez-Guillen D, Castillo-Vera A (2012) Infección natural de Lutzomyia cruciata (Diptera: Psychodidae, Phlebotominae) con Wolbachia en cafetales de Chiapas, México. Acta Zool Mex 28(2):401–413
Montes de Oca-Aguilar AC, Mikery-Pacheco O, Castillo A, Rebollar-Téllez EA, Piermarini P, Ibáñez-Bernal S (2017) Morphological variation of Lutzomyia cruciata eggs (Diptera: Psychodidae: Phlebotominae) in southern Mexico. Zootaxa 4258(5):477–489. https://doi.org/10.11646/zootaxa.4258.5.5
Moo-Llanes D, Ibarra-Cerdeña C, Rebollar-Téllez EA, Ibáñez-Bernal S, González C, Ramsey JM (2013) Current and future niche of North and Central American sand flies (Diptera: Psychodidae) in climate change. PLoS One 7:e2421. https://doi.org/10.1371/journal.pntd.0002421
Morrone JJ, Escalante T, Rodríguez-Tapia G (2017) Mexican biogeographic provinces: map and shapefiles. Zootaxa 4277(2):277–279. https://doi.org/10.11646/zootaxa.4277.2.8
Oguz G, Kasap OE, Alten B (2017) Wing morphology variations in a natural population of Phlebotomus tobbi Adler and Theodor 1930. J Vector Ecol 42(2):223–232
Ono M, Braig HR, Munstermann LE, Ferro C, O’Neill SL (2001) Wolbachia infections of phlebotomine sandflies (Diptera: Psychodidae). J Med Entomol 38(2):237–241. https://doi.org/10.1603/0022-2585-38.2.237
Pech-May A, Escobedo-Ortegón FJ, Berzunza-Cruz M, Rebollar-Téllez EA (2010) Incrimination of four sandfly species previously unrecognized as vectors of Leishmania parasites in Mexico. Med Vet Entomol 24(2):150–161. https://doi.org/10.1111/j.1365-2915.2010.00870.x
Pech-May A, Marina C, Vázquez-Domínguez E, Berzunza-Cruz M, RebollarTellez EA, Nárvaez-Zapata JA, Moo-Llanes D, Ibáñez-Bernal S (2013) Genetic structure and divergence in populations of Lutzomyia cruciata, a phlebotomine sand fly (Diptera: Psychodidae) vector of Leishmania mexicana in southeastern Mexico. Infect Genet Evol 16:254–262. https://doi.org/10.1016/j.meegid.2013.02.004
Pech-May A, Peraza-Herrera G, Moo-Llanes DA, Escobedo-Ortegón J, Berzunza-Cruz M, Becker-Fauser I, Montes de Oca-Aguilar AC, Rebollar-Téllez EA (2016) Assessing the importance of four sandfly species (Diptera: Psychodidae) as vectors of Leishmania mexicana in Campeche, México. Med Vet Entomol 30(3):310–320. https://doi.org/10.1111/mve.12169
Pérez J, Virgen A, Rojas JC, Rebollar-Téllez EA, Castillo A, Infante F, Mikery O, Marina CF, Ibáñez-Bernal S (2014) Species composition and seasonal abundance of sandflies (Diptera: Psychodidae: Phlebotominae) in coffee agroecosystems. Mem Inst Oswaldo Cruz 109(1):1–7. https://doi.org/10.1590/0074-0276130224
Prudhomme J, Gunat F, Rahola N, Ouanaimi F, Guernaoui S, Boumezzough A, Bañuls AL, Sereno D, Alten B (2012) Wing size and shape variation f Phlebotomus papatasi (Diptera: Psychodidae) populations from the south and north slopes of the Atlas Mountains in Morocco. J Vector Ecol 37(1):137–147. https://doi.org/10.1111/j.1948-7134.2012.00210.x
Prudhomme J, Cassan C, Hide M, Toty C, Rahola N, Vergnes B, Dujardin JP, Alten B, Sereno D, Bañuls AL (2016) Ecology and morphological variations in wings of Phlebotomus ariasi (Diptera: Psychodidae) in the region of Roquedur (Gard, France): a geometric morphometrics approach. Parasit Vectors 9(1):578. https://doi.org/10.1186/s13071-016-1872-z
Ramírez-Barahona S, Torres-Miranda A, Palacios-Ríos M, Luna-Vega I (2009) Historical biogeography of the Yucatán Peninsula, Mexico: a perspective from ferns (Monilophyta) and lycopods (Lycophyta). Biol J Linnean Soc 98(4):775–786. https://doi.org/10.1111/j.1095-8312.2009.01331.x
Ranasinghe S, Maingon RDC, Bray DP, Ward R, Udagedara C, Dissanayake M, Jayasuriya V, de Silva NK (2012) A morphological distinct Phebotomus argentipes population from active cutaneos leishmaniasis foci in central Sri Lanka. Mem Inst Oswaldo Cruz 107(3):402–409. https://doi.org/10.1590/S0074-02762012000300016
Rangel EF, Laison R, Souza AA, Ready P, Azevedo ACR (1996) Variation between geographical population of Lutzomyia (Nyssomyia) withmani (Antunes & Cautinho, 1939) sensu lato (Diptera: Psychodidae: Phlebotominae) in Brazil. Mem Inst Oswaldo Cruz 91(1):43–50. https://doi.org/10.1590/S0074-02761996000100007
Rebollar-Téllez EA, Reyes-Villanueva F, Fernández-Salas I, Andrade-Narváez F (1996) Abundance and parity rate of Lutzomyia cruciata (Diptera: Psychodidae) in an endemic focus of localized cutaneous leishmaniasis in southern Mexico. J Med Entomol 33(4):683–685. https://doi.org/10.1093/jmedent/33.4.683
Rohlf FJ (2007) TpsDig, Program for Digitalizing morphologic landmark and outlines for geometric morphometric analyses, version 2.04. Department of Ecology and Evolution, State University of New York, Stony Brook
Rzedowski J (1978) Vegetación de México. Limusa, México City, p 431
Saltelli A, Chan K, Scott EM (2000) Sensitivity analysis, vol 1. Wiley, New York
Sánchez-García L, Berzunza-Cruz M, Becker-Fauser I, Rebollar-Téllez EA (2010) Sand flies naturally infected by Leishmania (L.) mexicana in the peri-urban area of Chetumal city, Quintana Roo, México. Trans R Soc Trop Med Hyg 104(6):406–411. https://doi.org/10.1016/j.trstmh.2010.01.010
Sheets HD (2002) Semiland. A tool for processing semi-landmarks. Physics Department, Canisius College, Buffalo, New York, http://www.canisius.edu/~sheets/morphsoft.html. Accessed 15 Mar 2015
Sheets HD (2003) MakeFan. Available from http://www3.canisius.edu/~sheets/. Accessed 15 Mar 2015
Sheets HD (2005a) CoordGen, Coordinate Generation program for calculating shape coordinates. http://www3.canisius.edu/~sheets/morphsoft.html. Accessed 15 Mar 2015
Sheets HD (2005b) PCAGen, Principal components analysis based on partial warp scores, outputs partial warps scores and principle axis score. http://www3.canisius.edu/~sheets/morphsoft.html. Accessed 15 Mar 2015
Sheets HD (2005c) CVAGen, Canonical Variates Analysis program for the analysis of shape, based on partial warp scores. http://www3.canisius.edu/~sheets/morphsoft.html. Accessed 15 Mar 2015
Sheets HD (2005d) RegressGen, Regression tools for landmark data. http://www3.canisius.edu/~sheets/morphsoft.html. Accessed 15 Mar 2015
Sheets HD (2005e) DisparityBox, Investigating morphological disparity. http://www3.canisius.edu/~sheets/morphsoft.html. Accessed 15 Mar 2015
Sheets HD, Zeldich ML (2001) Tmorphgen6 traditional morphometrics variables generation utility part of IMP Integrated Morphometrics Package. Physics Department, Canisius College, Buffalo, New York, http://www.canisius.edu/~sheets/morphsoft.html. Accessed 15 Mar 2015
Shimabukuro PHF, Andrade AJ, Galati EAB (2017) Checklist of American sand flies (Diptera, Psychodidae, Phlebotominae): genera, species, and their distribution. ZooKeys 660:67–106. https://doi.org/10.3897/zookeys.660.10508
Srinivasan R, Jambulingam P (2012) Morphological and anatomical variations among Phlebotomus (Phlebotomus) papatasi sensu lato (Diptera: Psychodidae). J Med Entomol 49(3):441–444. https://doi.org/10.1603/ME11105
Thorpe RS (2009) Geographic variation: a synthesis of cause, data, pattern and congruence in relation to subespecies, multivariate analysis and phylogenesis. Boll Zool 54:3–11. https://doi.org/10.1080/11250008709355549
Vázquez-Domínguez E, Arita HT (2010) The Yucatán peninsula: biogeographical history 65 million years in the making. Ecography 33(2):212–219. https://doi.org/10.1111/j.1600-0587.2009.06293.x
Westh-Eberhard MJ (1989) Phenotypic plasticity and the origins of diversity. Annu Rev Ecol Syst 20:249–278. https://doi.org/10.1146/annurev.es.20.110189.001341
Young DG, Duncan AM (1994) Guide to the identification and geographic distribution of Lutzomyia sand flies in Mexico, the West Indies Central and South America (Diptera: Psychodidae. Mem Am Entomol Ins EE.UU 54:1–881
Zelditch ML, Swiderski DL, Sheets HD (2004) Geometric morphometrics for biologists: a primer. Elsevier Academic Press, London and New York
Zimmerman E, Palsson A, Gibson G (2000) Quantitative trait loci affecting components of wing shape in Drosophila melanogaster. Genetics 155(2):671–683
Acknowledgements
The first author (ACMOA) was supported by a graduate scholarship from the Mexican Council of Science and Technology (CONACYT, No. 414043). The present work was supported by project INECOL-10816 granted to SIB. We express our thanks to Maria Teresa Suarez Landa who helped in laboratory procedures. The helpful field assistance of Carlos Roberto García Torres, Mario Vázquez Márquez, Jorge Alberto Solis Hernández, Manuel Ramirez Castillo, Ignacio Alcazar Gómez, and David Moo-Llanes is also very much appreciated. We also thank three anonymous reviewers for significantly improving our manuscript.
Author information
Authors and Affiliations
Contributions
All five authors designed the study, ACMOA and EART collected the samples, ACMOA performed morphometric measurements of sampled material and data analyses, ACMOA and EL performed statistical analysis, ACMOA, EL and SIB wrote the manuscript, and all authors contributed in improving the draft of the manuscript by adding valuable comments.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All applicable international, national, and/or institutional guidelines for the care of participants in the field collection were followed.
Data accessibility
All data generated and analyzed during this study are included in this published article and its supplementary information files.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Montes de Oca-Aguilar, A.C., De Luna, E., Rebollar-Téllez, E.A. et al. Morphological discontinuous variation and disparity in Lutzomyia (Tricholateralis) cruciata Coquillett, 1907 are not related to contrasting environmental factors in two biogeographical provinces. Zoomorphology 138, 335–348 (2019). https://doi.org/10.1007/s00435-019-00450-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00435-019-00450-8