A case of gynandromorphism in Amblyomma mixtum (Acari, Ixodidae)

  • Fredy A. Rivera-Páez Universidad de Caldas
  • Marcelo B. Labruna Universidade de São Paulo-USP
  • Thiago F. Martins Universidade de São Paulo-USP
  • Bruno Rodrigues-Sampieri Departamento de Biologia, Instituto de Biociências, Universidade Estadual Paulista-UNESP, Rio Claro
  • María I. Camargo-Mathias Universidade Estadual Paulista-UNESP

Resumen

Gynandromorphism is a condition in which an organism simultaneously exhibits male and female morphological characteristics. In Colombia, the taxon Amblyomma cajennense is represented by the species Amblyomma patinoi and Amblyomma mixtum. In September of 2014, in the Colombian Orinoco region, adult ticks were collected and determined from natural infections in bovines and equines. A gynandromorph was described from a natural infestation on a bovine, and morphologically classified as A. mixtum. This is the first literature report of a gynandromorph of A. mixtum, and the first description of a gynandromorph for a tick species in Colombia.

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Publicado
2017-12-31
Como citar
RIVERA-PÁEZ, Fredy A. et al. A case of gynandromorphism in Amblyomma mixtum (Acari, Ixodidae). Revista Colombiana de Entomología, [S.l.], v. 43, n. 2, p. 268-270, dic. 2017. ISSN 0120-0488. Disponible en: <http://revistas.univalle.edu.co/index.php/SOCOLEN/article/view/5956>. Fecha de acceso: 19 sep. 2018 doi: https://doi.org/10.25100/socolen.v43i2.5956.
Sección
Notas científicas

Palabras clave

Biology, ticks, Neotropic

Introduction

Until a few years ago, the taxon Amblyomma cajennense (Fabricius, 1787) represented a single tick species distributed from southern United States to northern Argentina (Estrada-Peña et al. 2004). Recently, the taxon was reorganized into a complex of six valid species: A. cajennense sensu stricto (Fabricius, 1787) (restricted to the Amazonian region), Amblyomma mixtum Koch, 1844 (from Texas to western Ecuador), Amblyomma sculptum Berlese, 1888 (northern Argentina, Bolivia, Paraguay, Brazil), Amblyomma interandinum Beati, Nava and Cáceres, 2014 (inter-Andean valley of Peru), Amblyomma tonelliae Nava, Beati and Labruna, 2014 (dry areas of northern Argentina, Bolivia, and Paraguay), and Amblyomma patinoi Labruna, Nava and Beati, 2014 (Eastern Cordillera of Colombia) (Beati et al. 2013; Nava et al. 2014). In Colombia, this species complex is currently represented by A. patinoi (Nava et al. 2014) and A. mixtum (Rivera-Páez et al. 2016). Nevertheless, the current knowledge of the distribution of these species in America is likely incomplete and a species-level definition is necessary (Nava et al. 2014). At least three species of the complex, namely A. sculptum, A. mixtum, and A. patinoi, are important vectors of the bacterium Rickettsia rickettsii, the causal agent of the Rocky Mountain spotted fever, the deadliest tick-borne bacterial disease of the world (Krawczak et al. 2014; Labruna et al. 2014; Faccini-Martínez et al. 2015).

Gynandromorphs are individuals that possess phenotypic characteristics of males and females, and have been reported in several insect, spider, and tick taxa (Eritja 1996; Labruna et al. 2002). Their maturation begin during embryonic development, due to a loss of or damage to sex chromosomes, binucleated eggs, or infections related to Wolbachia species, a common endosymbiont (Narita et al. 2010; Keskin et al. 2012). Gynandromorphism in ixodid ticks is little known, but the phenomenon has been extensively reviewed and approximately 77 naturally-occurring cases have been documented (Prusinski et al. 2015). In the genus Amblyomma, over 20 cases have been reported among nine species, including A. cajennense, from which two cases have been reported (Labruna et al. 2002). Based on the geographical origin (southeastern Brazil) of these cases in A. cajennense, they are likely to correspond to A. sculptum. To date, no descriptions or records of gynandromorph presence have been reported in ticks in the Colombian territory.

Material and methods

During a field study on ticks infesting domestic animals in the Colombian Orinoco region, Arauca municipality, Arauca department (07°3’55”N, 70°44’2”W) during September of 2014 (Rivera-Páez et al. 2016), the presence of a gynandromorphy specimen of A. mixtum was noticed and collected from a cow (Bos taurus). The gynander was taxonomically evaluated (Jones et al. 1972; Nava et al. 2014), through a light microscope (Leica M205C stereomicroscope) and a scanning electron microscope (SEM) (Hitachi Scanning Electron Microscope, model TM3000) following techniques described by Corwin et al. (1979).

Results and discussion

All male and female specimens in the Orinoquía region of Colombia (Rivera-Páez et al. 2016) presented external morphological characters of A. mixtum, the males of A. mixtum the principal diagnostic character is the tick body outline, round in A. mixtum and oval in A. patinoi (Figs. 1A, 2A) and females of A. mixtum can be differentiated from females belonging to the other species of the group by the combination of notal setae stout and long, more densely distributed on the posterior half of the notum (Fig. 2A), small tubercles (Fig. 2A), and a U-shaped genital aperture with 2 narrow lateral flaps (Nava et al. 2014). Dorsally, the gynandromorph of A. mixtum showed the left idiosoma with male characteristics and a right idiosoma with typical female characteristics. Conversely, the capitulum possessed female traits at both sides, including a pair of porose areas and equal-sized palps (Figs. 1A, 2A-2B). A dorsal midline separated the scutum in the male side, where it covered the alloscutum, and the female side showed a reduced scutum, typical of females (Figs. 1A, 2A). The scutum of the specimen showed typical female ornamentation and punctations on the right side, and typical male ornamentation and punctuations on the left side as well (Figs. 1A, 2A). The dorsal midline ended at the middle of the sixth festoon, which had male and female halves corresponding to the rest of the dorsal area. A distinct complete lateral groove, typical of A. mixtum males, was also present at the male half (Figs. 1A, 2A). Ventrally, the results support those observed at the dorsal view, with a left side that corresponds to the typical male, and a right side corresponding to female, with the ventral midline extending from the capitulum to the sixth festoon (Figs. 1B, 2C). The spurs on coxae I-III were typical of the corresponding sex on each side; conversely, coxa IV spur is typically male at both sides, corresponding to a single long, stout, pointed spur (Figs. 1B, 2C-2D).

(A) Dorsal and (B) Ventral view of Amblyomma mixtum gynandromorph. (cs) coxal spur, (fe) festoons, (mg) marginal groove, (pal) palps, (scu) scutum.

Figure 1: (A) Dorsal and (B) Ventral view of Amblyomma mixtum gynandromorph. (cs) coxal spur, (fe) festoons, (mg) marginal groove, (pal) palps, (scu) scutum.

Scanning Electron Microscopy (SEM) of Amblyomma mixtum gynandromorph. A. dorsal view. B. dorsal basis capitulum. C. ventral view. D. ventral basis capitulum. (a) anal aperture, (cs) coxal spur, (fe) festoons, (ga) genital aperture, (mg) marginal groove, (h) hypostome, (pal) palps, (pa) porose area, (scu) scutum, (se) setae.

Figure 2: Scanning Electron Microscopy (SEM) of Amblyomma mixtum gynandromorph. A. dorsal view. B. dorsal basis capitulum. C. ventral view. D. ventral basis capitulum. (a) anal aperture, (cs) coxal spur, (fe) festoons, (ga) genital aperture, (mg) marginal groove, (h) hypostome, (pal) palps, (pa) porose area, (scu) scutum, (se) setae.

According to previous definitions of the types of gynandromorphism in ticks (Campana-Rouget 1959), the gynandromorph of A. mixtum described in this study is classified as a gynander intriqué of a protogynander, which means that the external sex-linked features are equally represented, except for ‘‘islands’’ of male or female chitin embedded in areas of the opposite sex. In the present specimen, these “islands” are present in the capitulum (mostly of the female type) at the male side, and at coxa IV of the female side. The most common type of gynandromorphism is a bipartite protogynander, whereas gynander intriqué is very rare in ticks (Labruna et al. 2002; Keskin et al. 2012). Among the genus Amblyomma, the bipartite protogynander is indeed the most common type of gynandromorphism (Labruna et al. 2002; Campana-Rouget 1959).

This research represents the first record of a tick gynandromorphin Colombia, and the first for A. mixtum.

Acknowledgements

Acknowledgements

AUIP- Asociación Universitaria Iberoamericana de Postgrado. CNPq- Conselho Nacional de Desenvolvimento Científico e Tecnológico. FAPESP- Fundação de Amparo a Pesquisa do Estado de São Paulo. Unidad Administrativa Especial de Salud de Arauca- Programa ETV Gobernación de Arauca (Colombia).

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