Triatominae As a Model of Morphological Plasticity Under Ecological Pressure JP Dujardin/+, P Panzera*, CJ Schofield**
Total Page：16
File Type：pdf, Size：1020Kb
Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 94, Suppl. I: 223-228, 1999 223 Triatominae as a Model of Morphological Plasticity under Ecological Pressure JP Dujardin/+, P Panzera*, CJ Schofield** UMR CNRS-ORSTOM 9926, ORSTOM BP 5045, 911 Av. Agropolis, Montpellier cedex 1, France *Sección Genetica Evolutiva, Facultad de Ciencias, Universidad de la Republica, Montevideo, Uruguay **Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London WC1 E7HT, UK The use of biochemical and genetic characters to explore species or population relationships has been applied to taxonomic questions since the 60s. In responding to the central question of the evolu- tionary history of Triatominae, i.e. their monophyletic or polyphyletic origin, two important questions arise (i) to what extent is the morphologically-based classification valid for assessing phylogenetic relationships? and (ii) what are the main mechanisms underlying speciation in Triatominae? Phenetic and genetic studies so far developed suggest that speciation in Triatominae may be a rapid process mainly driven by ecological factors. Key words: Triatominae - ecological factors - morphological plasticity ECOLOGICAL FORCES AND MORPHOLOGICAL pho-species which converged by adaptation to the PLASTICITY same ecotope (both are currently found in brome- Among the first attempts to examine other char- liads and in peridomestic habitats). But because acteristics than morphological traits in Triatominae any particular niche tends to be occupied by a single the use of haemolymph electrophoresis raised a species, sibling species would be less frequent in new taxonomic question by showing two distinct Triatominae than in other groups as Diptera where populations within Triatoma sordida (Actis et al. they may arise abruptly from a single mutation. 1964). Thirty-three years later, T. sordida was con- Unlike Diptera, chromosomes of Triatominae are firmed as a complex of isomorphic species both holocentric, accepting some damages without le- by cytogenetic and isoenzymatic techniques thal consequences (Maudlin 1976) and often with (Panzera et al. 1997, Noireau et al. 1998). These marked intraspecific polymorphism of heterochro- studies showed for the first time that significant matin content (Panzera et al. 1992). biochemical differences could subdivide a The idea that sibling species in Triatominae recognised morpho-species of Triatoma into dif- reflect morphological convergence, is supported ferent genetic units, although no other sibling spe- by observation of the morphological, metric and cies of Triatominae have yet been demonstrated. genetic changes of various species in the transi- The apparent rarity of sibling species in tion from silvatic to domestic habitat (Dujardin Triatominae may reflect the lack of relevant popu- 1998a/d). The sensory system, for example, in lation studies (Frias & Dujardin 1996), but could terms of the density of antennal sensilla, becomes also reflect the biological mechanism of sibling progressively simplified in accordance with in- species formation, especially if such mechanism creasing habitat stability (Catalá 1997); bilateral implied morphological convergence between two symmetry becomes relaxed (Fig. 1) (Dujardin & related species competing within the same ecologi- Casini 1996), as does sexual dimorphism (Fig. 2) cal niche. In this hypothesis, the sibling species of (Dujardin et al. 1999a); and a general reduction in sordida may initially have been two different mor- body size may also be seen (Dujardin et al. 1997a,b, 1998b,c, 1999b). Since morphology seems clearly modulated by ecological factors, we may assume that these same factors may produce divergent morphologies within This work benefited from international co-operation through the ECLAT network. a single species, or amongst closely related spe- +Corresponding author. Present address: Department of cies. A well documented example comes from Tropical Diseases, IBBA, ORSTOM La Paz, Casilla analysis of relationships between three species: T. Postal 9214 La Paz, Bolivia. Fax: +591-2-22.5846/ infestans, T. platensis and T. delpontei. T. infestans 24.3782. E-mail: [email protected] is well known as the main vector of Chagas dis- Received 9 June 1999 ease in the Southern Cone of South America, where Accepted 9 August 1999 it is typically found in the cracks and crevices of 224 Triatominae: Model of Morphological Plasticity JP Dujardin et al. FA 8 Rhodnius domesticus 7 6 4.17LF (4) 4.33 5 4 4.17 LM (4) 4.33 3 2 1 4.17 FF (8) 4.33 0 A BCDEH 4.17 FM (6) 4.33 Triatoma sordida, G2, 18 domestic specimens Triatoma infestans, 12 female domestic specimens Triatoma infestans, 20 male domestic specimens Triatoma infestans Fig. 1: values of fluctuating asymmetry (FA) corrected for mea- surement error according to Palmer and Strobeck (1986). G2, one of the two sibling species of Triatoma sordida. Silvatic speci- 4.71FD (33) 4.84 mens of T. sordida are not visible on the figure since they showed no significant asymmetry. All these specimens were kindly pro- vided by F Noireau, IRD. 4.71MD(40) 4.84 poor quality rural houses, emerging at night to feed on the sleeping occupants. In contrast, T. platensis 4.71MS (20) 4.84 and T. delpontei are ornithophilic arboreal species, quite unimportant in the transmission of human Chagas disease (Salvatella 1986, 1987). T. platensis 4.71 FS (10) 4.84 commonly infests the woven stick nests of furnariid weaver birds (Anumbius spp.) in northern Argen- Fig. 2: female (F) and male (M) specimens of Rhodnius tina, Paraguay, Uruguay and southern Brazil, but domesticus (top), either reared in laboratory (LF, LM) or re- has also been found in peridomestic habitats such cently collected in the field (FF, FM), aligned along the first principal component (PC1) as an estimator of global size (head as chicken coops. T. delpontei seems more eco- measurements). Female (F) and male (M) specimens of Triatoma logically restricted, found almost exclusively in infestans (bottom), collected in house (FD, MD) or in silvatic woven stick nests of colonial monk parrots ecotopes of Cochabamba (FS, MS), aligned along the PC1as (Myiopsitta monarcha), but occupying a similar an estimator of global size (head measurements). geographical range to T. platensis. The genetic dis- tance computed for 24 electrophoretic loci was higher between the morphologically and ecologi- cally similar T. platensis and T. delpontei than be- quicker than the installation of reproductive or tween T. platensis and T. infestans, raising ques- genetic barriers. This latter idea is not new: it was tions about the evolutionary relationships between formulated by Usinger et al. (1966) as the conclu- these species previously derived from morphologi- sion of many interfertility experiments. It was con- cal traits (Pereira et al. 1996). Moreover, the isoen- tained also in the conclusion of Gorla et al. (1997) zyme studies were in agreement with previous in- suggesting a New World origin of the Old World terfertility (Usinger et al. 1966) and cytogenetic Triatoma. According to these authors, the New studies (Panzera et al. 1995), and was recently con- World members of the genus Triatoma would have firmed by DNA studies (García & Powels 1998). T. rubrofasciata as unique ancestor. This species This case study, as well as the rapid morpho- seems to have been spread from the Americas a logical changes associated with domestic adapta- few centuries ago, and subsequently specialised tions, suggested that ecological factors may be the into the seven recognised species of Triatoma main force driving speciation in Triatominae found in the Asian region (Gorla et al. 1997). This (Pereira et al. 1996). More importantly, it also sug- iconoclastic idea relies on the assumption of rela- gested that morphological differentiation could be tively rapid morphological changes. Mem Inst Oswaldo Cruz, Rio de Janeiro, Vol. 94, Suppl. I, 1999 225 EVOLUTIONARY IMPLICATIONS 7.38 Rapid morphological changes – either conver- gent or divergent – associated with ecological ad- S aptation, help to explain discordance between ge- netic and phenetic differentiation, and provides a Triatoma new basis for developing the species concept in melanosoma Triatominae. D Ecological species 6.67 Species with consistent morphological differ- 9.85 10.74 ences would arise through divergent ecological cv1 adaptation. In other words, morphological species 3.643 of Triatominae would be “ecological species”, a vision which fits with the concept of “evolution- ary units” (Wiley 1989) where two populations S become different species if they follow distinct Triatoma infestans evolutionary fates. Such an idea does not preclude Paraguay the existence of important genetic differences, but implies a different evolutionary direction taken by D some populations. The idea implies that recent “evolutionary units” would be still very close ge- 3.133 7.175 7.98 netically, which is probably the case of the T. cv1 infestans, T. platensis and T. delpontei species group described above. Fig. 3: discriminant analyses of wing shape showing that dif- ferences between Bolivian Triatoma infestans, either domestic This could also be the case of T. infestans and (D) or silvatic (S) ones, and T. melanosoma (top) are compat- T. melanosoma. T. infestans melanosoma Martínez, ible with simple geographic variation within T. infestans (bot- Olmedo & Carcavallo 1987 has been recently el- tom). S: silvatic sample of T. infestans (19 wings) from evated to species rank