1. Art and Diseño

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Discussion
Triatoma dimidiata (Latreille, 1811): A review of its diversity across
its geographic range and the relationship among populations
Patricia L. Dorn a,*, Carlota Monroy b, Andrew Curtis c
a
Department of Biological Sciences, Loyola University New Orleans, 6363 St. Charles Ave. New Orleans, LA 70118, USA
b
LENAP, University of San Carlos, 12 calle 11-71 zona 2, Ciudad Nueva, Guatemala, Central America
c
Department of Geography and Anthropology, Howe-Russell Complex, Louisiana State University, Baton Rouge, LA 70803-4105, USA
Received 31 July 2006; received in revised form 30 September 2006; accepted 3 October 2006
Abstract
Due to its vast diversity the Chagas vector, Triatoma dimidiata, has been merged and split into species and subspecies since its first description
in 1811. Across its geographic range from Southern Mexico to Northern Peru populations differ in their biology and ethology in many ways
including those that directly affect vector capacity and competence. Recent phenetic and genetic data suggest that T. dimidiata can be divided into
at least three clades and in fact may be a polytypic species or species complex. To effectively target this vector, it will be necessary to clearly
understand how ‘‘T. dimidiata’’ is genetically partitioned both at the taxonomic and population level.
# 2006 Elsevier B.V. All rights reserved.
Keywords: Chagas disease; Triatoma dimidiata; Ecology; Ethology; Genetics; Phenetics; Phylogeny; ITS2
1. Introduction
1.1. The importance of correct identification for control
efforts
The Chagas vector, Triatoma dimidiata (Latreille, 1811), is a
highly variable species with a wide geographic range: from
Mexico through Central America into Venezuela, Colombia,
Ecuador and northern Peru. The origin of the species appears to
be Southern Mexico/Northern Guatemala (Schofield, 2002). It
is currently the main Chagas vector in Guatemala, El Salvador,
Nicaragua and Costa Rica, and the second most important
vector in Honduras and Colombia. Control of the species must
take into account its enormous variation and the diversity of its
habitat which includes numerous types of sylvatic, peridomestic and domestic ecotopes (Petana, 1971; Zeledo´n et al.,
1973; Monroy et al., 2003b). Differences among populations of
T. dimidiata have a direct effect on control, e.g. in some areas of
Nicaragua reinfestation is not observed after insecticide
spraying (Acevedo et al., 2000) however, in other areas, such
* Corresponding author. Tel.: +504 865 3672; fax: +504 865 2920.
E-mail addresses: [email protected] (P.L. Dorn),
[email protected] (C. Monroy), [email protected] (A. Curtis).
as Jutiapa in Guatemala, reinfestation confounds control efforts
(Nakagawa et al., 2003b). From the beginning of the Central
America Initiative for the interruption of the vectorial
transmission of Chagas Disease, IPCA (OPS, 1997), it was
clear that T. dimidiata is not susceptible to elimination.
Therefore, assuming the continued presence of the vector, the
goal is to reduce the domiciliary infestation of T. dimidiata
(OPS, 1999) and avoid human infection with Trypanosoma
cruzi, the causative agent of Chagas disease (OPS, 2002).
T. dimidiata belongs to a group of Reduviid insects that are
found in sylvatic and artificial environments (woodpiles,
chicken coops, etc.) and also found colonizing houses as
evidenced by the presence of eggs and nymphs as well as adults
(Schofield, 2002). The control strategies must take into
consideration the degree of adaptation of the species to human
dwellings (OPS, 2002). T. dimidiata populations from Peru and
Ecuador seem to be exclusively domestic and peridomestic
(Arzube, 1966; Schofield, 2002), possibly introduced by sea
trade during Pre-Columbian times (Schofield, 2002). The lack
of evidence of sylvatic populations in Northern Peru and
Ecuador (Abad-Franch et al., 2001) contrasts with numerous
sylvatic populations in Southern Mexico, Belize, Northern
Guatemala, Nicaragua and Costa Rica (Petana, 1971; Zeledo´n
et al., 2001b; Dumonteil et al., 2002; Monroy et al., 2003b).
Highly domesticated populations are susceptible to elimination
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Please cite this article in press as: Dorn, P.L. et al., Triatoma dimidiata (Latreille, 1811): A review of its diversity across its geographic range and
the relationship among populations, Infect. Genet. Evol. (2006), doi:10.1016/j.meegid.2006.10.001
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whereas it is unlikely sylvan populations can be eliminated
(Monroy et al., 1998b). It is also clear that not all sylvatic
populations are genetically related to the domestic ones
(Caldero´n et al., 2004), implying reproductive isolation,
although in some areas domestic and sylvan populations are
panmictic (Ramirez et al., 2005). In some areas reinfestation is
rapid (less than 6 months) following insecticide application,
e.g. Yucatan, Mexico (Dumonteil et al., 2004), Jutiapa,
Guatemala (Nakagawa et al., 2003b), and Nicaragua (Schofield, 2005). Whereas in other areas reinfestation is not a
problem, e.g. in Zacapa, Guatemala (Nakagawa et al., 2003a).
For control purposes, those populations that remain sylvatic are
not relevant as disease vectors; however, the epidemiological
importance of those that re-infest from peridomestic and/or
sylvan habitats will require development of new strategies for
their control (Ramirez et al., 2005).
Vector Control Programs are aimed at reducing the prevalence
of the vector and must vary with the species of vector implicated
and transmission cycle. Control strategies for T. dimidiata need to
be designed in light of the biological and genetic differences of
what appears to be a polytypic species (i.e., consists of distinct
subspecies varying with geographical distance yet able to
interbreed) (Bustamante et al., 2004), or even a complex of
cryptic species (reproductively isolated species that are
morphologically indistinguishable) (Jurberg et al., 2005; Panzera
et al., 2006). We need to understand what all is included under the
umbrella of ‘‘T. dimidiata’’ and which variants play major or
minor roles in the transmission of Chagas to humans. For control
purposes we need to understand how the variability of the species
effects observed different outcomes of control.
The morphological variation of T. dimidiata across its
distribution has been well known since the first description of
the species; variation that historically has led to considerable
splitting, merging and name changes (Table 1). More recently,
Pifano and Ortiz revised the group dimidiata excluding
Triatoma capitata of Venezuela from the species. They also
provide a description of a ‘‘mexicana-dimidiata group’’,
associating T. mexicana with T. capitata and T. hegneri with
T. maculipennis and T. dimidiata (Pifano and Ortiz, 1973).
Lent and Wygodzinsky (1979) analyzing 160 specimens
from Belize, El Salvador, Guatemala, Nicaragua, Costa Rica,
Panama, Colombia, Venezuela, Ecuador and Peru conclude
that, ‘‘T. dimidiata has not segregated into clearly separable
allopatric populations: the observable differences are roughly
clinal in nature, but many specimens are difficult to place’’.
Only recently taxonomists have suggested that, due to the
enormous variation of coloration, external features and size, T.
dimidiata is more aptly considered a species complex (Jurberg
et al., 2005). Here we summarize the considerable body of work
that documents the vast differences among T. dimidiata
populations across its geographic range and what is known
about the relationship among different populations.
Table 1
Historical Classification of Triatoma dimidiata by morphological characters
Year
Names
Comments
References
1811
Reduvius dimidiatus
von Humboldt and Bonpland (1811)
1859
Conorhinus
1868
1882
1899
1914
C. dimidiatus
C. maculipennis
C. dimidiatus maculipennis
Triatoma dimidiatus maculipennis
1921
1925
T. dimidiata maculipennis
T. dimidiata
1933
T. dimidiata maculipenies
1931–1941
T. dimidiata and T. maculipennis
First description of the species, thought from
Peru, later source was determined to be Ecuador
Two very similar species described: C. dimidiatus
from Ecuador, Costa Rica, Panama
and C. maculipennis from Mexico
C. dimidiatus and C. maculipennis synonymized
Used for specimens from Mexico
maculipenis considered as subspecies of dimidiatus
Included is the genus Triatoma as subspecies.
Rejected separation of species, and recommend
the use of the oldest name
Accepted the designation of subspecies
T. dimidiata and T. dimidiata maculipennis
synonymized
maculipennis should remain a subspecies of
T. dimidiata as many intermediate specimens found
Considered separate species
1941
T. dimidiata, T. maculipenis,
T. capitata
1944
T. dimidiata, T. d. maculipenis,
T. d. capitata
1967
T. dimidiata maculipenis
1960–1978
T. dimidiata ‘‘complex’’
1979
T. dimidiata, T. d. maculipenis,
T. d. capitata
T. capitata described in Colombia. Created the
group ‘‘dimidiata’’ with T. hegneri, T. capitata,
T. dimidiata and T. maculipennis as distinct species
Usinger changes 1941 designation and now
considers maculipennis and capita subspecies
of T. dimidiata
Populations from Yucatan T. dimidiata and
T. dimidiata maculipennis are interbreeding
T. dimidiata ‘‘complex’’ included two
subspecies, maculipennis and capitata
The differences are clinal, all belong
to same species
Stahl (1859)
Stahl (1868)
Stahl (1859), Lent and Wygodzinsky (1979)
Champion (1899)
Neiva (1914)
Del Ponte (1921)
Pinto (1925)
Bequart (1933)
Pinto (1931), Lent and Wygodzinsky
(1979), Neiva and Lent (1936, 1941)
Usinger (1941)
Lent and Jurberg (1985)
Gonzalez-Angulo and Ryckman (1967)
Lent and Jurberg (1985)
Lent and Wygodzinsky (1979)
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the relationship among populations, Infect. Genet. Evol. (2006), doi:10.1016/j.meegid.2006.10.001
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2. Biology and ethology of T. dimidiata
2.1. Life zones and ecosystems
T. dimidiata populations are found in diverse life zones and
ecosystems. In Costa Rica sylvan T. dimidiata occupies at least
eight life zones (Holdridge, 1967) including the very hot and
humid premontane forest with the greatest abundance of bugs
followed by the humid tropical forest (Zeledo´n et al., 2001b).
However, in Guatemala, the vector is most abundant in the dry,
tropical forest near the border with El Salvador (Tabaru et al.,
1999; Monroy et al., 2003a). The species is more plentiful
around the altitude of 1000 meters above sea level (m.a.s.l.) but
it can be found from 0–1750 m.a.s.l. in Guatemala (Tabaru
et al., 1999) and 1000–2000 m.a.s.l. in Costa Rica (Zeledo´n
et al., 2001b).
Triatominae distribution appears to be strongly influenced
by climate (temperature, precipitation, humidity). In Yucatan,
Mexico, T. dimidiata is more abundant in warmer and dryer
climates while in Oaxaca, Mexico it seems to be restricted to
regions with milder temperatures (Dumonteil and Gourbiere,
2004). Prediction models using climatological factors seem to
accurately predict distribution of the species in Yucatan
(Dumonteil and Gourbiere, 2004); however, in Guatemala
populations are widespread, differ greatly and climatic factors
do not accurately predict distribution (Bustamente et al.,
unpublished data).
2.2. Dispersion by flight and colonization
The capacity for movement of T. dimidiata is evidenced by
human blood in insects found in the peridomestic environment
(Arzube, 1966; Zeledo´n et al., 1973), domestic and wild animal
blood found in bugs inside houses (Sasaki et al., 2003) and the
colonization of artificial ecotopes (Zeledo´n et al., 2001a;
Monroy et al., 2003b). However, while some populations show
a high propensity for movement, others appear not to migrate
beyond the immediate surroundings.
Nocturnal flight by T. dimidiata was first reported in 1931,
associated with the introduction of public electricity in
Guayaquil, Ecuador (Campos, 1931). Flight was also reported
early on in Yucatan, Mexico (Paloma, 1940) and in Costa Rica,
a male was reported flying into a Shannon light trap (Rosabal,
1969).
Some populations appear to remain sylvan, e.g. in Belize
(Petana, 1971) and in Pete´n, Guatemala (Tabaru et al., 1999;
Monroy et al., 2003b) domestic infestation is very low; the few
bugs caught in houses seem to have been attracted to the lights
at night. It is believed that the populations in these areas are
well established in their outdoor ecotopes and feed on the
variety of readily available animals in the forest.
There is evidence that certain populations migrate between
sylvan and domestic habitats, e.g. in Costa Rica (Zeledo´n et al.,
1973), Northern (Pete´n) Guatemala (Monroy et al., 2003b),
Belize (Petana, 1971) and Yucatan, Mexico, (Quintanal and
Polanco, 1977). In Colombia, sylvan T. dimidiata seems to be
interbreeding with domestic populations so must be considered
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epidemiologically important (Ramirez et al., 2005). Seasonality of flight migration into houses is evident in some
populations and usually occurs between March and September, with highest levels in Costa Rica in April and May
(Zeledo´n et al., 2001b), April–June in the Yucatan (Dumonteil
et al., 2002) and May and June in Northern Guatemala, before
the rainy season (Monroy et al., 2003b). However, for T.
dimidiata from caves in El Cayo District, Belize, the peak of
abundance is during the rainy season, August and September
(Petana, 1971).
In other localities it appears that T. dimidiata is mainly a
domestic and peridomestic vector, e.g. Zacapa, Jutiapa,
Guatemala; Madriz, Nicaragua and Guayaquil, Ecuador
(Arzube, 1966; Acevedo et al., 2000; Nakagawa et al.,
2003a,b).
The urban presence of the species is well documented in
several cities such as Merida, Mexico; Caracas, Venezuela;
Tegucigalpa, Honduras; San Jose and Heredia, Costa Rica
(Zeledo´n and Rabinovich, 1981); Guayaquil, Ecuador
(Izquieta, 1968). The urban presence is a feature of the
dispersion and colonization of the species which requires novel
approaches to control.
2.3. Habitat diversity and blood source preference
Different populations of T. dimidiata have been found in
distinct microhabitats such as under cow dung, in the bark of
dead trees (Campos, 1931), in caves occupied by bats, in rock
piles, Mayan ruins, hollow trees, and nests of several mammals
such as opossums and armadillos (Petana, 1971; Zeledo´n and
Rabinovich, 1981; Monroy et al., 2003b). Palm trees are also
reported as habitat for the species in Panama, Guatemala, and
Costa Rica (Whitlaw and Chaniotis, 1978; Vargas, 1985;
Monroy et al., 2003b). Some sylvan specimens from Belize and
Guatemala were found in limestone caves and rock piles and
associated with bats, snakes, lizards and rodents (Petana, 1971;
Monroy et al., 2003b; Bustamante et al., 2004).
In domestic infestation there are also different preferences in
resting sites. In Mexico, the species is often found more
commonly at floor level (Guzman-Bracho, 2001), and in Costa
Rica, a change from dirt floor to concrete nearly eliminated the
vector inside houses (Zeledo´n and Vargas, 1984). In Guatemala,
the vector is more abundant on the walls, rather than the floors,
and wall improvements reduced the density in the house
(Monroy et al., 1998b).
Populations of T. dimidiata also differ as regards their
blood meal preference. T. dimidiata from Ecuador has a
marked preference for rats (Arzube, 1966). Mammals and
birds are popular in Western Panama where mammalian
feeding comprised 74% (mostly humans and dogs) and birds
25%. Opossum blood was not found (Christensen et al., 1988).
Birds are important as well in Yucatan, Mexico where T. d.
maculipennis preferred birds (chickens) as a primary blood
source (Quintanal and Polanco, 1977). Bugs also from the
Yucatan collected inside houses showed similar feeding
preferences for humans and birds (Guzma´n-Marin et al.,
1992).
Please cite this article in press as: Dorn, P.L. et al., Triatoma dimidiata (Latreille, 1811): A review of its diversity across its geographic range and
the relationship among populations, Infect. Genet. Evol. (2006), doi:10.1016/j.meegid.2006.10.001
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A wide range of blood sources have been reported in T.
dimidiata from Costa Rica (Rosabal, 1969; Zeledo´n et al.,
1973, 2005; Zeledo´n and Rabinovich, 1981) and Guatemala
(Sasaki et al., 2003) including several mammals, birds, toads
and snakes, although most studies report human blood as the
most prevalent meal for bugs found in domestic and
peridomestic sites.
In contrast, several specimens collected in sylvan opossum
nests harbored only opossum blood (Zeledo´n et al., 1970).
Interestingly, under laboratory conditions wild caught T.
dimidiata from Belize refused to feed on human volunteers
and preferred animal hosts (animals from caves), showing the
sylvan habits in the British Honduras populations (Petana,
1971).
2.4. Infestation rates
The size of natural populations of Triatomines is closely
related to the density of the host on which the bugs feed
(Schofield and Matthews, 1985). The number of T. dimidiata
inside houses is regulated by the availability of blood sources;
houses with fewer inhabitants showed a lower number of bugs
(Monroy, unpublished data). In storerooms and wood piles a
greater number of bugs were collected likely due to the
presence of a significant number of rodents and synanthropic
animals (Zeledo´n et al., 1975). The highest number of
specimens recorded comes from a storeroom in Costa Rica
where 1861 specimens were collected (Zeledo´n, 1981); while
in whole house demolition experiments in Guatemala, lower
numbers were found, 100–300 per house (Monroy et al.,
1998a). Usually a low number of specimens (1–10) is
collected from each house using the person/h method, i.e. one
person searching for 1 h or two people for 0.5 h (Zeledo´n,
1981).
There are large differences in infestation (number of bugs
found in a locality) and dispersion (number of localities
infested in a region) across T. dimidiata populations. The
dispersion index (the percentage of villages infested with the
vector in a province or state) is extremely high in Yucatan,
Mexico (95%, Guzman-Marin et al., 1991), very high also in
eastern Guatemala (Jutiapa 86%, Tabaru et al., 1998) and El
Salvador (Santa Ana 80%, Sonsonate 89% and Ahuachapan
67%, OPS, 2004) and about half this level in northern
Guatemala (Quiche 33% and Alta Verapaz 40%, Tabaru et al.,
1998). The domestic infestation index in Yucatan, Mexico
appears to be one of the highest in the region (61%, GuzmanMarin et al., 1991), followed by Sonsonate, El Salvador (40%,
OPS, 2004), while the highest in Guatemala is found in Jutiapa
(35%, Tabaru et al., 1998).
The sex ratio in sylvan populations shows more males
than females on the island of Barro Colorado in Panama
(Sousa et al., 1983), in Pete´n, Guatemala (Monroy et al.,
2003b), and in Costa Rica in sylvan populations collected by
light traps (Zeledo´n et al., 2001b). However, in the caves in
Lanquin, Alta Verapaz, Guatemala, females are more
abundant than males (Monroy et al., 2003b; Bustamante
et al., 2004).
2.5. Life cycle of T. dimidiata originating in Mexico, Costa
Rica, Ecuador and Colombia
The length of the life cycle depends on temperature,
humidity and availability of blood sources. Under laboratory
conditions T. dimidiata from different regions seems to have
different life spans. In Costa Rica and Guatemala, the life
cycle is approximately one generation per year (384–397
days from egg to adult in Costa Rica, Zeledo´n, 1981;
Zeledo´n et al., 1970; Monroy et al., 2003b). One hundred day
shorter life cycles have been reported in Mexico (Guzma´nMarin et al., 1992), Colombia (Otalora, 1952) and Ecuador
(Arzube, 1966). In Colombia sylvan T. dimidiata capitata
had a very short life cycle, about two generations per year
(196–210 days, Otalora, 1952), similar to that seen in
Ecuador (220 day from egg to egg, Arzube, 1966).
However, as the length of the lifecycle depends on the
conditions of the experiment, e.g. the density of the
population, it may be that the differences observed are not
innate to the populations but instead due to experimental
conditions.
Adults of T. dimidiata maculipennis from Yucatan take, on
average, 24 min to start defecating following a blood meal
(Guzma´n-Marin et al., 1992). And thus have likely left the
host before releasing live parasites in the feces. T. dimidiata
from Costa Rica takes a shorter time to defecate (11 min) so
may transmit a bit better than the Yucatan population.
However, this is also a timid species that is frequently
interrupted while feeding allowing less time to leave parasiteladen feces on the host (Zeledo´n et al., 1977). The defecation
pattern of the populations may explain some of the
differences in seroprevalence in humans found in different
regions.
2.6. T. cruzi infection rates
Infection rates with T. cruzi also were different among
different populations of T. dimidiata. In the Yucatan, at
different times and in different localities infection rates were
reported to be: 0% in Tipoco, 16.6% in Merida and 25% in rural
Tella (Paloma, 1940), or 16% in seven municipalities in the
state of Yucatan (Guzman-Marin et al., 1991). There is some
evidence that in different ecological zones, the natural
infection rate with the parasite differs, e.g. in Guatemala,
the domestic populations from the departments of Santa Rosa
showed 29.1%, Jutiapa 9.7% and Chiquimula 11.5% infection
rates (Monroy et al., 2003a). A much higher rate of infection
with T. cruzi was found in Santander, Colombia: 48% of T.
dimidiata were found infected (Angulo et al., 1999) and in
Guayaquil, Ecuador, 50% infected (Go´mez-Lince, 1968). In
San Jose, Costa Rica the infection rate varies from district to
district, 28.8% in Santa Ana and 47.5% in Pozos (Chinchilla
and Montero-Gei, 1967). The sylvan T. dimidiata from Pete´n,
northern Guatemala showed an infection rate of 25% (Monroy
et al., 2003b), while under the same sylvatic conditions 43% of
the bugs in the island Barro Colorado, Panama harbored T.
cruzi (Sousa et al., 1983).
Please cite this article in press as: Dorn, P.L. et al., Triatoma dimidiata (Latreille, 1811): A review of its diversity across its geographic range and
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2.7. Factors affecting human transmission
Clearly many of these factors have a direct effect on the
rates of T. cruzi transmission to humans. More competent T.
cruzi vectors show a high degree of adaptation to human
dwellings (including a possible preference for human blood
and/or tolerance of the bug saliva by humans) and high rates
of infestation and crowding within domiciles. High rates of
infection with the parasite, rapid defecation following the
blood meal and a long lifespan which allows a longer time to
transmit the parasite also contribute to significant transmission rates. High rates of dispersion whether active (by
walking or flight), or passive, e.g. due to human activity or
carriage of eggs by migrating birds also contribute to this
public health threat. Any or all of these factors (and host
factors as well) can affect seroprevalence rates. Indeed, in
humans in areas where T. dimidiata is the predominant vector
these rates vary considerably. Very low rates have been
reported from blood donors in Quiche, Guatemala 0%, (Matta
et al., 1994), 0–1.7% in Yucatan, Mexico (Quintanal and
5
Polanco, 1977), 1.5% overall in Mexico (Guzman Bracho
et al., 1998) and 4.2% in children less than 10 years old from
Santa Maria Ixhu´atan, Santa Rosa, Guatemala (Villagran de
Tercero et al., 1993). Much higher rates are seen, e.g. 8.9% in
Primera Sabana, Santa Rosa, Guatemala (Paz-Bailey et al.,
2002) to 7.1%, 10% and 18.5%, respectively, in blood donors
from Escuintla, Santa Rosa and Chiquimula, Guatemala
(Matta et al., 1994). In Costa Rica, among 1420 persons
examined, 11.7% were seropositive for T. cruzi (Zeledo´n
et al., 1975).
Thus, there is tremendous diversity in the biology and
ethology of T. dimidiata across its geographic range and this
diversity has led different investigators, or the same investigator
at different times, to split or merge species and subspecies or
even create groups for T. dimidiata (Table 1). The current
working definition of a single species showing a clinal variation
is being called into question with recent data so it is important
to again address the question of the relationships of different T.
dimidiata populations using the newer phenetic and genetic
tools we now have available.
Fig. 1. A geographic variation measure among Triatoma dimidiata populations was achieved by adding the total difference for each location based on the
total number of nucleotides that differed from the consensus at each position of sequence as a proportion of the difference within that position. Therefore,
if one location has a different nucleotide at a certain position, a value of 1/n, whereby n = the total number of other locations also displaying a different
nucleotide, is calculated and these are added over all 478 nucleotides. The difference measure is classified into four classes using natural breaks,
which minimizes the variance between cluster groups. *Unpublished sequences (Dorn et al.), GenBank Accession numbers: DQ871354, DQ871355,
DQ871356.
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the relationship among populations, Infect. Genet. Evol. (2006), doi:10.1016/j.meegid.2006.10.001
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2.8. Relationships of different populations based on
phenetic studies
2.8.1. Geographic proximity correlates with phenetic
relatedness
Results of several phenetic studies suggest geographic
proximity correlates with the relatedness of populations. For
example, cuticular hydrocarbon analysis of Mexican T.
dimidiata populations showed a clustering among isolates
from Southern Mexico (Hidalgo, Veracruz and part of Oaxaca);
the next most closely related populations were from Chiapas
(Calderon-Fernandez et al., 2005b, locations in Fig. 1). Vera
Cruz clustered with adjacent states by antennal phenotype (with
Hidalgo, Catala´ et al., 2005) and by morphometry of head
characters (with San Luis Potosı´, Lehmann et al., 2005). Thus,
geographically close Southern Mexico populations are clustered by these phenetic characters, a pattern that is repeated in
Central America by morphometry of heads. Here canonical
variant analysis polygons generated from head characters of
populations from Central Guatemala and Honduras overlap
(Quiche´, Alta Verapaz, Santa Rosa, Guatemala and Yoro,
Honduras, Fig. 2; Bustamante et al., 2004).
However, two populations are completely unrelated to
other nearby populations. By cuticular hydrocarbons,
populations from the southern foothills of the Sierra Madre
Oriental were entirely separate from all other Mexican
populations, including Oaxacan populations from the
northern foothills of the same mountain range. Instead, the
southern Oaxacan population clustered with domestic southern Guatemalan populations Jutiapa and Santa Rosa; the
authors suggest a recent introduction of Central American
bugs (Calderon-Fernandez et al., 2005b). And in Guatemala,
by morphometry and cuticular hydrocarbons, the sylvan
populations from caves in Lanquin, Alta Verapaz, Guatemala
are quite separated from all other T. dimidiata populations,
including those elsewhere in Alta Verapaz. Instead they are
most closely related to isolates from Boavita, Colombia
Fig. 2. Canonical variate analysis over three ‘‘allometry free’’ components in
head characters of females comparing eight Triatoma dimidiata populations
from different geographic origins. The two canonical factors (CF1 and CF2)
together represented 99.3% (86.0 and 13.3%, respectively). Reprinted from
(Bustamante et al., 2004).
(Bustamante et al., 2004; Calderon-Fernandez et al., 2005a).
Here the authors suggest that habitat may play a role in the
similarity; although the Boavita insects were collected inside
houses, they appear to have originated in nearby caves and are
also associated with the peridomestic environment (Bustamante et al., 2004). In fact, the Lanquin and Boavita isolates
are as different from other T. dimidiata populations as a
different species (Bustamante et al., 2004; CalderonFernandez et al., 2005a,b).
The region encompassing the Yucatan peninsula and
northwest Guatemala is the oldest geological region in the
Central America (C.A.) isthmus formation (Coates, 1997). Its
fauna and flora seem to be related to the northern hemisphere
but there was a great interchange with the south as well (Webb,
1997). The complexity of the geology of the Central American
Isthmus is manifest in the variety of terrains, ecosystems,
asymmetry of geological structures and contrasts greatly from
the northern and southern hemispheres. Schofield (2005)
postulated that T. dimidiata may have originated in the Yucatan
peninsula, dispersing from there into isolated populations
which diverged into species such as T. hegneri in Cozumel and
T. flavida in Cuba (Schofield, 2005). By analysis of cuticular
hydrocarbons, Yucatan populations are separate from all other
Mexican populations except for overlap with those from the
nearby island of Cozumel (Calderon-Fernandez et al., 2005b).
By morphometry, the Yucatan populations cluster with those
from the Pete´n, Guatemala (Lehmann et al., 2005) and by
cuticular hydrocarbons, Pete´n, in turn, clusters with Cozumel
and the Yucatan (Calderon-Fernandez et al., 2005b), again all
within some geographic proximity. In addition, sylvan and
domestic Yucatan isolates cluster by cuticular hydrocarbons
suggesting that at least for these populations, proximity is more
important than habitat in predicting relatedness (CalderonFernandez et al., 2005b). The one exception is the antenna
phenotype data which shows the domestic Yucatan isolates
clustering with the domestic isolates from Southern Mexico
(Hidalgo and Vera Cruz; Catala´ et al., 2005).
Thus, with rare exceptions, the phenetic evidence shows a
southern Mexico cluster, a Central American cluster and
Northern Guatemala (Pete´n) and Yucatan, Mexico as a cluster,
quite separate from the others.
2.8.2. Little evidence for a major role of habitat in
relatedness of populations
In rare instances, habitat may play a stronger role in
relatedness than geographic proximity, especially when
analyzing the antennal phenotype. Perhaps this is a character
particularly susceptible to habitat influence. In contrast to
cuticular hydrocarbon and morphometry data (described
above), the antenna phenotype showed clustering of domestic
Yucatan samples with other domestic Mexican populations
from Hidalgo and Veracruz (Catala´ et al., 2005). In addition,
antennal phenotype clearly distinguishes populations from
three distinct habitats, sylvan-forest (Pete´n, Guatemala) sylvancaves (Lanquin, Alta Verapaz, Guatemala), and domestic
populations from Guatemala and Honduras (Catala´ et al.,
2005). These results are mirrored by cuticular hydrocarbon data
Please cite this article in press as: Dorn, P.L. et al., Triatoma dimidiata (Latreille, 1811): A review of its diversity across its geographic range and
the relationship among populations, Infect. Genet. Evol. (2006), doi:10.1016/j.meegid.2006.10.001
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showing sylvan-forest (Pete´n, Guatemala), sylvan-cave (Lanquin, Alta Verapaz, Guatemala) and Guatemalan domestic
populations completely separate (Calderon-Fernandez et al.,
2005a). Although populations may be separated based on
distinct habitats, these populations are also geographically far
apart suggesting that distance and not habitat is the overriding
factor. In addition, from morphometry and cuticular hydrocarbon data it is clear that the cave population is quite distinct
from all other isolates, in fact may be a completely separate
species (C. Monroy, unpublished data).
Arguing against habitat having a major role in relatedness,
by morphometry sylvan Pete´n isolates overlapped with the
domestic populations, although the Lanquin (sylvan-cave)
populations are still separate (Calderon-Fernandez et al.,
2005a). Therefore, although some results support the role of
habitat in selection for relatedness, most of the phenetic data
does not.
2.9. Relationship of populations based on genetic studies
The genetic structure of T. dimidiata across its geographic
range has been analyzed using several molecular methods
including: sequencing regions of the T. dimidiata genome
(specifically the internal transcribed spacer 2, ITS2), cytogenetics and determining DNA content, by randomly amplified
polymorphic DNA-PCR (RAPD-PCR) and isoenyzme analysis.
Results show the differences in allele frequencies between
populations, Nei’s genetic distance (D) (Nei, 1972), or genetic
differentiation as a result of separation and genetic drift,
Wright’s F ST (Wright, 1978). Qualitatively, an F ST value less
than 0.05 indicates little differentiation, a value of 0.05–0.15
indicates moderate differentiation, and 0.15–0.25 great
differentiation, and greater than 0.25 indicates very great
differentiation (Wright, 1978).
2.9.1. Nearby populations
In SE Guatemala (Jutiapa), where T. dimidiata is almost
exclusively domestic, RAPD-PCR revealed that populations
within one house and one village were panmictic with a low
genetic distance and little genetic differentiation (D = 0.018;
F ST = 0.025) (Dorn et al., 2003). In addition, populations from
nearby villages 27 km apart were also interbreeding
(D = 0.0199; F ST = 0.019) (Dorn et al., 2003). However, in
Colombia, where domestic, peridomestic and sylvan populations exist in close proximity, moderate genetic differentiation
was observed by RAPD-PCR among different ecotopes
separated by only 200 m (F ST = 0.070) although allele
frequencies had not diverged significantly (D = 0.0078–
0.011). Thus it appears that, like T. infestans, the size of the
panmictic unit may differ in different geographic regions. It
may be that the distinct habitats (as seen in the Colombian
populations) allow more separation of populations. Clearly
more studies are needed as so far only two localities have been
analyzed. Additional markers with more sensitivity like
microsatellites may show population subdivision previously
undetected by RAPD-PCR (Dorn et al., 2004).
7
2.9.2. Populations from different departments
RAPD-PCR has also been used to examine population
structure across different departments in Guatemala. Results
revealed moderate genetic differentiation among domestic
populations (D = 0.072; F ST = 0.097) and a higher genetic
distance and the higher end of moderate differentiation among
sylvan populations from different departments (D = 0.161;
F ST = 0.135). However, due to the difficulty of obtaining sylvan
samples, the sample size was quite low so conclusions must be
considered preliminary. Across Guatemala and the two
ecotopes, great genetic differentiation was observed
(F ST = 0.175; Caldero´n et al., 2004). This is consistent with
the high amount of genetic variability seen as high levels of
polymorphism by isoenzyme analysis in specimens from two
different states in Mexico, Oaxaca and San Luis Potosı´
(P(0.95) = 0.5) (Flores et al., 2001). Therefore, increasing
population differentiation correlates with greater geographic
distance, consistent with the isolation by distance model
(Dujardin et al., 1988).
2.9.3. Populations from different countries
Differentiation among populations from different countries
has been examined by comparing the sequence of the internal
transcribed spacer 2 (ITS2), part of the rDNA repeat. As the
region is spliced out and degraded to produce the 5.8S and 28S
rRNAs immediately following transcription, selection on its
sequence probably just involves folding into the correct
secondary structure to allow accurate processing. Therefore it
shows a relatively high rate of mutation which has made it a
useful marker for species, subspecies and even population level
analyses (Coleman, 2003). Results comparing ITS2 sequences
showed that within different states in Mexico (Oaxaca,
Morelos, Veracruz and San Luis Potosı´) ITS2 sequences from
different specimens were nearly identical (Marcilla et al.,
2001). However, comparing these sequences from Mexico, 7–
10 differences were identified with those from Honduras and
Nicaragua which are, in turn, three nucleotides different from
each other. Interestingly, the Honduras sequence is identical to
that of the specimen from Ecuador suggesting a recent
introduction event into Ecuador. As seen with phenetic
characters, Yucatan specimens are as different from the others
as a different species (Marcilla et al., 2001). The authors
propose a ‘‘clinal variation’’ from S. Mexico through Central
America although recent data suggests the existence of at least
three clades: the Yucatan, Mexico and Pete´n, Guatemala (with
identical ITS2 sequence), another from S. Mexico through N.
Guatemala and the third extending south through at least
Honduras, El Salvador and Nicaragua (Dorn, et al., unpublished
data; Fig. 1).
Recent cytogenetic analysis distinguishing ‘‘cytotypes’’
based on the amount, location and behavior of C-heterochromatin during meiosis and mitosis and DNA content showed
slightly different subdivisions. Cytotype I was found in domestic
and peridomestic individuals from northern and southern
Guatemala (excluding Pete´n), El Salvador, southern Mexico
(excluding the Yucatan) and Colombia. Cytotype II was found in
the Yucatan, Mexico and Cytotype III in the Pete´n region of
Please cite this article in press as: Dorn, P.L. et al., Triatoma dimidiata (Latreille, 1811): A review of its diversity across its geographic range and
the relationship among populations, Infect. Genet. Evol. (2006), doi:10.1016/j.meegid.2006.10.001
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P.L. Dorn et al. / Infection, Genetics and Evolution xxx (2006) xxx–xxx
Guatemala (Panzera et al., 2006). Different samples were used
here than those used for ITS2 analysis. However, these results
may indicate that there are at least two reproductively isolated
populations in the Pete´n region—one more similar to bugs in the
Yucatan and one distinct from those. These results have direct
epidemiological implications as the ones from the Yucatan
appear to invade houses, at least seasonally, so that house
treatments are important for control (Dumonteil et al., 2002). In
Pete´n, populations appear to remain sylvan so are not important
epidemiologically (Monroy et al., 2003b).
Thus, from what limited genetic data is available, and not
surprisingly, it appears that populations in close proximity are
more related than more distant populations. However, the size
of the panmictic unit may differ in different regions and may
depend on the availability of different habitats. On the broader
geographical scale, there is clear population structuring
consistent with the ‘‘isolation by distance’’ model proposed
by Dujardin et al. (1988). It must be emphasized that there is a
minimum of data on which these preliminary conclusions are
based and more studies must be conducted to resolve the
population structuring of T. dimidiata. As ITS2 and the
cytogenetic data are currently showing different population
subdivisions (with regards to Pete´n and the Yucatan), it will be
important to analyze additional specimens and perhaps use
different markers to resolve these differences and clarify finer
subdivisions, e.g. between northern and southern Guatemala.
As both the bulk of the phenetic and genetic data point to
clades encompassing: (1) Southern Mexico, (2) the Yucatan and
part of Pete´n, Guatemala and (3) the remainder of Central
America, it is not surprising that populations near to a putative
border region sometimes cluster with one side or the other (e.g.
Pete´n). It will be important to elucidate the boundaries of
distinct populations and to understand the mechanism of
population subdivision. Accordingly, more populations from
Southern Mexico and Northern Guatemala and between
Northern Guatemala and the Yucatan peninsula should be
collected and typed for phenetic and genotypic characters. In
addition, much more needs to be learned about South American
populations.
Thus, considerable variation has been documented for T.
dimidiata across its geographic range. Some of this variation,
e.g. degree of domesticity, infestation and infection rates with T.
cruzi, etc. directly affects transmission of Chagas. To aid the
Central American and Andean initiatives to halt Chagas
transmission, it will be necessary to clarify the different
epidemiological relevance of the putative T. dimidiata species,
subspecies and populations. For the countries that have sylvan
and domestic populations in the same region, i.e. Mexico,
Guatemala, El Salvador, Honduras, Nicaragua, Costa Rica,
Panama´ and Colombia, the control strategy includes clear
identification of the target population in the domestic and/or
sylvan environment and stratification of risk of reinfestation of
each population. Effective control efforts will require knowing
precisely which species is being targeted and the biology of that
population. To date, an understanding of the population
subdivisions of T. dimidiata including its characterization as
a polytypic species or species complex is in its infancy.
Community surveillance and stratification of the human
populations at risk have been proposed as control strategies to
target the populations most at risk for Chagas infection
(Schofield, 2005). Identification of the areas of highest
transmission risk will require application of phenetic and
genetic methods to the vector populations to understand the
origin of re-infesting populations, to be clear about the target
population and to understand the geographic coverage
necessary for effective control.
Acknowledgements
We are grateful to Drs. Donald Hauber and Bart Sefton for
critical review of the manuscript, to two anonymous reviewer
for helpful suggestions and to Dr. Rodrigo Zeledo´n for sharing
many articles and references.
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