Morphology of reproductive accessory glands in eight species of blood-feeding Hemiptera (Hemiptera, Reduviidae) insect vectors of Chagas disease

doi:10.1016/j.actatropica.2012.01.011

Acta Tropica

Volume 122, Issue 2, May 2012, Pages 196-204

https://doi.org/10.1016/j.actatropica.2012.01.011 Get rights and content

Abstract

This paper documents the morphology of previously undescribed adult reproductive accessory glands in eight species of blood-feeding Hemiptera, vectors of Chagas disease. These species are three Triatoma (T. dimidiata, T. klugi, T. sordida), three Rhodnius (R. brethesi, R. nasutus, R. pictipes), and one species each from Nesotriatoma (N. bruneri) and Panstrongylus (P. megistus). This survey shows that the male reproductive systems between species of four genera of Reduviidae adhere to the same general plan seen in previously described vectors of Chagas disease. This morphological similarity suggests that reproductive success of the male is contingent on the delivery of a vital set of male accessory gland secretions to the female in conjunction with material from the testes and seminal vesicle. However, variations were observed in the accessory glands of females, especially at the level of the genus. The spermathecae are morphologically distinct, and the posterior accessory glands are absent in some. The differences in spermathecae morphology likely reflect physiological adaptations associated with speciation driven by cryptic female choice in which the female determines which sperm are used for fertilization. Differences in the posterior reproductive accessory gland can be correlated with variations in ovipositioning behaviour. Since reproductive physiology is important for species success, this information also augments epidemiological studies by providing a comparison to R. prolixus, a Chagas disease vector for which the physiology is well known.

Graphical abstract

Morphological examination of living tissues from eight species of Chagas vectors showed that male reproductive accessory glands were similar between species, but female glands varied. Morphology of the reproductive accessory glands in three species of Triatoma. For each species, a picture of the male adult with wings removed is to the left, while the corresponding line diagrams of female and male reproductive systems are to the right of the photograph, with the female diagram in the middle and male to the far right. Note that the organs and glands of male reproductive system are bilaterally symmetrical and only the right side has been drawn in these figures. (A) Triatoma dimidiata, (B) T. klugi, and (C) T. sordida.

Highlights

► Reproductive accessory gland morphology is described in eight species of Chagas disease vectors. ► Comparison employs the same morphological techniques to describe living tissue. ► Males possess an accessory gland complex having the same number and types of glands. ► Females have spermathecae unique to the species providing a mechanism for cryptic female choice. ► This morphological comparison suggests that control methods targeting male reproduction may affect more than one vector species.

Introduction

After the Southern Cone Initiative (begun in 1991, see Dias, 2007) and other vector control programs in the Andes, Central America, Mexico and the Amazon, focussing on the principal vector, Triatoma infestans, the incidence of Chagas disease was significantly reduced. As a consequence of the success of these policies, Uruguay, Chile and Brazil received in 2006 the Pan American Health Organization (PAHO)/World Health Organization (WHO) certification for interruption of Triatoma infestans vector transmission (Lannes-Vieira et al., 2010). Nevertheless, vector borne transmission of T. cruzi still occurs in some Central and South American regions (Dias, 2009, Guhl et al., 2009), associated with indoor invasion and potential domiciliation of autochthonous triatomine species, representing a real obstacle in the prevention of T. cruzi transmission. Based on evidence that sylvatic species can adapt to environmental changes and inhabit domiciles (Dujardin et al., 1991, Dias et al., 2000), it has become important to fully understand the physiology of these species in efforts to control Chagas disease in the endemic countries.

Fortunately, one insect vector of Chagas disease, Rhodnius prolixus, is a popular model for the study of insect physiology. It has been used to document such physiological processes as endocrinology (Wigglesworth, 1933, Wigglesworth, 1934, Wigglesworth, 1939), feeding (Orchard, 2006), diuresis (Martini et al., 2007), reproduction (Davey, 2007), ecology (Chaves et al., 2004, Zeledon et al., 2006) and the insect's response to sensory cues (Schilman et al., 1996, Schilman and Lazzari, 2004, Abramson et al., 2005, Abramson et al., 2007). New insights continue to be discovered as more recently, Martens and Chiang (2010) reported on rhodtestolin, a testes factor able to inhibit contractions of the female heart in R. prolixus. The importance of R. prolixus to the advancement of scientific knowledge in general is exemplified by it being designated by the National Human Genome Research Institute (USA) as a strategic species for complete genome sequencing (Rhodnius Genome Sequencing Project initiated in 2005; see Huebner, 2007).

Considering the wealth of information on the physiology of R. prolixus, and its continued use as an insect model, it would be beneficial to have a better understanding of the applicability of its physiology to other vectors of Chagas disease. The information presently available from studies of other Chagas vectors suggests similarities in structure and function among these insects (for example, see Insausti, 1994, Freitas et al., 2010). Unfortunately, this information is limited since much of it is derived from studies having a different focus and using different scientific techniques. To provide a more robust comparison, the present study uses the same array of morphological techniques to investigate the anatomy of the reproductive system in eight species belonging to four genera of Reduviidae. In addition, this work describes recently dissected living tissue thereby reducing the morphological artefacts associated with preserved specimens. This approach has uncovered a number of similarities and differences in the reproductive systems of these insects. This information provides some insights that may prove important for designing future research endeavours to help develop effective control strategies for these important vectors of disease.

Section snippets

Insects and dissection

Adults of three species of Triatoma (T. dimidiata, T. klugi, T. sordida), three of Rhodnius (R. brethesi, R. nasutus, R. pictipes), and one each of Nesotriatoma (N. bruneri) and Panstrongylus (P. megistus) were examined in the laboratory facilities at the Institute of Oswaldo Cruz-Fiocruz, Rio de Janeiro, Brazil. These insects were obtained from colonies of the Laboratory of National and International Reference on Triatominae Taxonomy of that institute, and these colonies were established with

General features

After being placed in 70% ethanol, the colour of the stained tissues tended to change from different shades of blue to shades of green and purple. The structural integrity of the organs remained intact permitting comparisons to the freehand drawings of the live tissue. Example photographs of the preserved reproductive organs are provided in Fig. 1 for a female, and in Fig. 2 for a male.

In Fig. 3, Fig. 4, Fig. 5, photographs of the intact dorsal cuticle of representative males from the eight

Discussion

To cope with the many different types of environments in which they can be found, the reproductive physiology among the insects is quite diverse (for examples, see Wigglesworth, 1979, Chapman, 1998). Triatominae described in the present study do not live in extreme environments and require no special adaptations. In addition, their digestive systems are relatively simple since they are blood feeders obtaining their nutrients in an already digested form. Their sexual physiology is also simple

Acknowledgments

This work was supported in part by an Internal Research Grant and an Invited Travel Grant from RUC to RGC. The authors thank Dr. Cleber Galvão and Mrs. Vanda Cunha, of the Laboratory of National and International Reference on Triatominae Taxonomy, Fiocruz, for the insect species investigated in this study.

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Morphology of reproductive accessory glands in eight species of blood-feeding Hemiptera (Hemiptera, Reduviidae) insect vectors of Chagas disease

Abstract

Graphical abstract

Highlights

Introduction

Section snippets

Insects and dissection

General features

Discussion

Acknowledgments

Acta Trop.

J. Insect Physiol.

T. Roy. Soc. Trop. Med. H.

Exp. Parasitol.

Micron

J. lnsect Physiol.

Comp. Biochem. Phys. A

Tissue Cell

Tissue Cell

Comp. Biochem. Physiol.

Insect Biochem. Mol.

Insect Biochem.

J. Insect Physiol.

Acta Trop.

Psychology of learning: a new approach to study behavior of Rhodnius prolixus Stål under laboratory conditions

Psychol. Rep.

Exposure to citral, cinnamon and ruda disrupts the life cycle of a vector of Chagas disease

Am. J. Environ. Sci.

The transmission of Actinomyces rhodnii Erikson in Rhodnius prolixus Stål (Hemiptera) and its influence on the growth of the host

Parasitology

Endosymbiosis of Animals with Plant Microorganisms

The Insects

A newly discovered sperm transport system in the female of Lygaeidae bugs

Physiol. Entomol.

A novel receptor capable of monitoring applied pressure in the abdomen of an insect

Science

A sensory input inhibiting heart rate in an insect, Rhodnius prolixus

Experientia

Sperm ejection as a possible cryptic female choice mechanism in Odonata (Insecta)

Physiol. Entomol.