Research Article |
Corresponding author: Silvia A. Justi ( silvinhajusti@gmail.com ) Academic editor: Guanyang Zhang
© 2018 Patricia L. Dorn, Silvia A. Justi, Carolina Dale, Lori Stevens, Cleber Galvão, Raquel Lima-Cordón, Carlota Monroy.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Dorn PL, Justi SA, Dale C, Stevens L, Galvão C, Lima-Cordón R, Monroy C (2018) Description of Triatoma mopan sp. n. from a cave in Belize (Hemiptera, Reduviidae, Triatominae). ZooKeys 775: 69-95. https://doi.org/10.3897/zookeys.775.22553
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In this paper, Triatoma mopan sp. n. is described based on five males and six females collected in the Rio Frio cave, Cayo District, Belize. This species is similar to Triatoma dimidiata (Latreille), but can be distinguished by characters found on the pronotum, legs, and abdomen. Geometric morphometry and phylogenetic comparisons are also provided. Presently, the species is known only from the type locality and is a potential Chagas vector.
Belize, Chagas disease, new species, Triatoma dimidiata , Triatoma mopan
Species belonging to Triatominae Jeannel, 1919 (Insecta, Hemiptera, Reduviidae) are important as vectors of Chagas disease. Presently, more than 150 species within 15 genera (
Because of the substantial morphological variation of T. dimidiata across its large geographic distribution (southern Mexico to Peru), this species has been split and synonymized many times since its original description (reviewed in
Following the synonymizing of the species (
In this manuscript, we describe T. sp. aff. dimidiata – cave, the lineage from the Rio Frio cave, as Triatoma mopan sp. n. (Hemiptera, Reduviidae, Triatominae), a new species of the genus Triatoma.
We conducted field work on June 15, 2016 in the Rio Frio cave, Cayo District, Belize [(coordinates: 16.956939/-88.979675) under permits covering the research (#IA/H/1/16 (03), Institute of Archaeology), collecting (#WL/1/1/16 (33), Forest Department) and export (#WL/1/7/16 (29), Forest Department) of specimens from Belize. The sole purpose of this field work was to collect enough specimens from the Rio Frio cave Triatoma population to reliably compare this population with T. dimidiata from other localities. We collected specimens from the Rio Frio cave, Cayo, Belize because of previous results of phylogenetic studies that showed this population to be an independent lineage distinct from all other populations included under the umbrella of T. dimidiata, and to be the only phylogenetic species found in this particular cave. We collected 15 adult males and 13 adult females and more than 70 nymphs of various lifecycle stages. For this study, we focus on the adult morphology.
Adults collected in the Rio Frio cave could not be taxonomically identified using the key for Triatoma species (
Specimens used for morphological and morphometric comparison. CTIOC: Triatominae Collection of the Oswaldo Cruz Institute.
Species | Specimen origin | ID/voucher number | Geographic Origin | Sex | Notes |
---|---|---|---|---|---|
T. sp. aff. dimidiata | field | A10800 | Huehuetenango, Guatemala | F | |
field | A10727 | Huehuetenango, Guatemala | M | ||
Triatoma dimidiata s.l. | CTIOC | 2838 | Colombia | M | capitata morphotype |
Colony LNIRTT* | N/A | Colombia | F | capitata morphotype | |
CTIOC | N/A | Santa Boyaca, Colombia | F | capitata morphotype | |
CTIOC | 2463 | Costa Rica | F | ||
CTIOC | 2592 | Costa Rica | F | ||
CTIOC | 2587 | San Jose, Costa Rica | F | ||
Colony LNIRTT* | N/A | Equador | F | ||
Colony LNIRTT* | N/A | Equador – genitalia | M | ||
CTIOC | 3385 | Candelaria Caves, Alta Verapaz, Guatemala | M | ||
CTIOC | A6160 | Lanquin Caves, Guatemala | M | ||
CTIOC | 3388 | Lanquin Caves, Guatemala | M | ||
CTIOC | 3377 | Peten | M | ||
CTIOC | 3379 | Peten | F | ||
CTIOC | A9703 | Peten | F | ||
CTIOC | 8937 | Mexico | M | maculipennis morphotype | |
CTIOC | N/A | Peru | M | ||
CTIOC | 2769 | N/A | M | ||
California Academy of Sciences | N/A | Boyacá, Colombia | M | capitata holotype | |
Triatoma gerstaeckeri | CTIOC | 6242 | Mexico | F | |
CTIOC | N/A | San Marcos, Texas, US | M | ||
CTIOC | N/A | Texas | M | ||
CTIOC | 6239 | N/A | F | ||
CTIOC | 6241 | N/A | F | ||
Triatoma mopan | Colony 16 LNIRTT | N/A | Belize | F | colony started in 12/05/2006 |
Colony 147 LNIRTT | N/A | Belize | F | colony started in 12/05/2006 | |
Field | 2016BZ001 | Cayo District, Rio Frio Cave, | F | ||
Field | 2016BZ002 | Cayo District, Rio Frio Cave, Belize | F | ||
Field | 2016BZ003 | Cayo District, Rio Frio Cave, Belize | F | ||
Field | 2016BZ004 | Cayo District, Rio Frio Cave, Belize | F | ||
Field | 2016BZ005 | Cayo District, Rio Frio Cave, Belize | F | ||
Field | 2016BZ006 | Cayo District, Rio Frio Cave, Belize | F | ||
Field | 2016BZ007 | Cayo District, Rio Frio Cave, Belize | M | ||
Field | 2016BZ008 | Cayo District, Rio Frio Cave, Belize | M | ||
Field | 2016BZ009 | Cayo District, Rio Frio Cave, Belize | M | ||
Field | 2016BZ011 | Cayo District, Rio Frio Cave, Belize | M | ||
Field | 2016BZ013 | Cayo District, Rio Frio Cave, Belize | M |
Character observation and measurements were made with a stereoscopic Zeiss Stemi SV11 microscope, using a graduated eyepiece micrometer, and photos were taken using a Nikon Coolpix 990 digital camera. The following characters were measured:
TL total length of the body
LOP and WOP length and width of pronotum
AOR and POR length of the ante- and post-ocular region
SYN length of the inter-ocular region or synthlipsis
HL and WOH length and width of the head
WE width of the eye
TS total length of scutellum
POS length of process of scutellum
A1-A4 length of antennal segments
R1-R3 labial segments (Figure
The terminology and measurements used for the description were based on
Sequence information and specimens used for the phylogenetic reconstruction and calculation of genetic distances.
Taxon | Sequence ID | Locality | ITS-2 | Cyt b |
---|---|---|---|---|
T. dimidiata | 1 | Sta. Theresa, Toledo | DQ871354 | FJ197155 |
10 | Caserío la Bendición, Monte Largo, Santa Ana, El Salvador | AM286693 | JN585881 | |
11 | Caserío la Bendición, Monte Largo, Santa Ana, El Salvador | AM286693 | JN585881 | |
12 | Caserío la Bendición, Monte Largo, Santa Ana, El Salvador | AM286693 | JN585881 | |
13 | Caserío la Bendición, Monte Largo, Santa Ana, El Salvador | AM286695 | JN585881 | |
14 | Caserío la Bendición, Monte Largo, Santa Ana, El Salvador | KT874438 | JN585881 | |
15 | Sto. Tomás, Sto. Domingo, Heredia, Costa Rica | AM286693 | JN585893 | |
16 | Sto. Tomás, Sto. Domingo, Heredia, Costa Rica | AM286693 | JN585894 | |
17 | Sto. Tomás, Sto. Domingo, Heredia, Costa Rica | AM286693 | JN585894 | |
18 | Angeles, San Rafael, Heredia, Costa Rica | KF192843 | JN585894 | |
19 | Sto. Tomás, Sto. Domingo, Heredia, Costa Rica | KT874433 | JN585895 | |
2 | Mérida, Yucatán, Mexico | FJ197146 | FJ197157 | |
20 | Colombia | AM286703 | KT998309 | |
21 | Colombia | AM286703 | KT998309 | |
22 | Colombia | AM286704 | KT998309 | |
23 | Colombia | KF192845 | KT998310 | |
24 | Lanquin, Alta Verapaz, Guatemala | AM286702 | KT998313 | |
25 | Lanquin, Alta Verapaz, Guatemala | AM286702 | KT998314 | |
26 | El Lodo Negro, San Marcos Sierra, Intibuca, Honduras | AM286694 | KT998315 | |
27 | El Masical, San Antonio, Copán, Honduras | AM286694 | KT998316 | |
28 | El Masical, San Antonio, Copán, Honduras | AM286695 | KT998316 | |
29 | Caserío la Bendición, Monte Largo, Santa Ana, El Salvador | AM286693 | KT998317 | |
3 | Lanquin, Alta Verapaz, Guatemala | AM286694 | JN585861 | |
30 | Caserío la Bendición, Monte Largo, Santa Ana, El Salvador | AM286696 | KT998318 | |
T. dimidiata | 31 | El Lodo Negro, San Marcos Sierra, Intibuca, Honduras | AM286695 | KT998319 |
32 | El Masical, San Antonio, Copán, Honduras | AM286694 | KT998320 | |
33 | El Lodo Negro, San Marcos Sierra, Intibuca, Honduras | AM286693 | KT998321 | |
34 | El Lodo Negro, San Marcos Sierra, Intibuca, Honduras | KT874435 | KT998321 | |
35 | El Lodo Negro, San Marcos Sierra, Intibuca, Honduras | KT874437 | KT998321 | |
36 | El Masical, San Antonio, Copán, Honduras | AM286693 | KT998322 | |
37 | El Masical, San Antonio, Copán, Honduras | KT874436 | KT998322 | |
38 | El Lodo Negro, San Marcos Sierra, Intibuca, Honduras | AM286693 | KT998325 | |
39 | El Lodo Negro, San Marcos Sierra, Intibuca, Honduras | AM286694 | KT998325 | |
4 | Lanquin, Alta Verapaz, Guatemala | AM286702 | JN585861 | |
40 | El Lodo Negro, San Marcos Sierra, Intibuca, Honduras | AM286695 | KT998325 | |
41 | El Masical, San Antonio, Copán, Honduras | KT874434 | KT998325 | |
42 | Caserío la Bendición, Monte Largo, Santa Ana, El Salvador | AM286693 | KT998327 | |
43 | Angeles, San Rafael, Heredia, Costa Rica | AM286693 | KT998328 | |
44 | Sto. Tomás, Sto. Domingo, Heredia, Costa Rica | KT874432 | KT998330 | |
45 | Angeles, San Rafael, Heredia, Costa Rica | KF192844 | KT998331 | |
46 | San Pedro Columbia, Toledo district, Belize | FJ197153 | FJ197154 | |
5 | Caserío la Bendición, Monte Largo, Santa Ana, El Salvador | AM286693 | JN585881 | |
6 | Caserío la Bendición, Monte Largo, Santa Ana, El Salvador | AM286693 | JN585881 | |
7 | Caserío la Bendición, Monte Largo, Santa Ana, El Salvador | AM286693 | JN585881 | |
8 | Caserío la Bendición, Monte Largo, Santa Ana, El Salvador | AM286693 | JN585881 | |
9 | Caserío la Bendición, Monte Largo, Santa Ana, El Salvador | AM286693 | JN585881 | |
T. sp. aff dimidiata | 1 | Calla Creek, Cayo District, Belize | FJ197152 | FJ197156 |
2 | Mérida, Yucatán, Mexico | FJ197150 | FJ197158 | |
3 | Mérida, Yucatán, Mexico | FJ197147 | FJ197159 | |
4 | Teya, Yucatán, Mexico | KT874439 | KT998296 | |
5 | Huehuetenango, Guatemala | |||
5 | Huehuetenango, Guatemala | |||
T. mopan | 1 | Río Frio Cave, Cayo District, Belize | KF192846 | JN585883 |
2 | Río Frio Cave, Cayo District, Belize | KF192847 | JN585884 | |
Col16 | ||||
T. infestans | AJ576054 | JN006799 | ||
T. gerstaeckeri | Chihuahua | JQ282707 | JQ282723 | |
T. brailovskyi | Jalisco | JQ282704 | JQ282720 | |
T. hegneri | AM286727 | JN585830 |
Morphometric comparison of the dorsal portion of the heads was made based on eight landmarks (Figure
In order to compare the head shape variation between T. mopan and closely related taxa, we used eight landmarks (clear, visible, homologous intersections between structures;
Portions of the nuclear Internal transcribed spacer 2 (ITS-2) and mitochondrial cytochrome b (cytb) gene sequences from all nominal species belonging to the dimidiata species subcomplex and species affinis (T. dimidiata, T. sp. aff. dimidiata, T. gerstaeckeri, T. brailovskyi, T. hegneri, and T. mopan; Table
Sequences were aligned using MAFFT version 7 (
In order to evaluate previously reported genetic distances (
Holotype Male. BELIZE: Cayo: Rio Frio Cave, coordinates: 16.956939/-88.979675, 15 June 2016, Dorn, Justi, Stevens, Monroy, CTIOC, FIOCRUZ. Paratypes. Five males and six females, Cayo: Rio Frio Cave, coordinates: 16.956939/-88.979675, 15 June 2016, Dorn, Justi, Stevens, Monroy (CTIOC; FIOCRUZ [four males and five females]; National Museum of Natural History, Smithsonian Institution [one male and one female])
Triatoma mopan has an overall vestiture similar to T. dimidiata, generally with a more slender body. It is believed to have been wrongly identified as T. dimidiata by
Length of male 26.6–30.1 mm., of female 32.1–38 mm.; width of pronotum of male 6.2–6.3 mm., of female 6–7.4 mm (Table
Head distinctively rugose dorsally (Figure
Neck dark, with 1+1 lateral light brown to yellowish spots. Pronotum uniformly dark brown to black, with a distinctive depression forming a straight latitudinal line from the neck to the posterior portion of the pronotum (Figure
Abdomen ventrally convex, minutely striate transversally, with scarce yellow pilosity. Mostly dark brown, with yellow spots extending from the connexival suture (Figure
External genitalia dark brown to black, almost round, with setae darker than the rest of the tegument in males; triangular, with long reddish setae on females (Figure
To date, the species is only known from the type locality.
Rio Frio cave, Cayo District, Belize, coordinates 16.956939/-88.979675.
The specific epithet mopan was chosen to honor the indigenous Mopan people, one of the Mayan groups historically and presently in this area of Belize and Guatemala, and comprises the lineage previously referred to as T. sp. aff. dimidiata (Group 4 – cave;
Specimens of T. mopan sp. n. collected prior to its description, in the same Rio Frio cave, were found to be infected with Trypanosoma cruzi (Monroy, unpublished data). The type series was not investigated for parasite infection in order to preserve the integrity of the samples.
Earlier studies completed by our research group, identifying blood sources on specimens of the then undescribed T. mopan collected in the same Rio Frio cave indicate that this species feeds on human, pig, goat or sheep, rat, mouse, duck, bat, opossum, and synanthropic and wild vertebrates (
Found in caves, in cracks in rocks near water, in humid environment.
Character measures used for the description were compared separately for males and females between T. mopan and the morphotypes of T. dimidiata (Table
Character measurements (mm) of T. mopan and T. dimidiata specimens and significance of t-test results for the comparison between the sexes of both species. Key: asterisk (*) significant value based on Benjamini-Hochberg multiple comparison False Discovery Rate, FDR = 0.05. n.s. non-significant value, N/A – not available.
Character | T. mopan females | T. dimidiata females | T. mopan males | T. dimidiata males | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
N | Mean (mm) | Min–Max (mm) | N | Mean (mm) | Range (mm) | P-value | N | Mean (mm) | Range (mm) | N | Mean (mm) | Range (mm) | P-value | |
A1 | 6 | 1.63 | 1.406–1.781 | 6 | 1.492 | 1.200–1.750 | n.s. | 5 | 1.538 | 1.406–1.625 | 6 | 1.223 | 1.000–1.563 | < 0.02* |
A2 | 6 | 4.719 | 4.500–5.281 | 5 | 4.2 | 3.400–4.800 | n.s. | 5 | 4.769 | 4.125–5.313 | 4 | 4.255 | 4.000–4.719 | n.s. |
A3 | 3 | 4.365 | 4.219–4.531 | 3 | 3.567 | 3.100–3.800 | n.s. | 5 | 4.194 | 3.688–4.469 | 0 | N/A | N/A | N/A |
A4 | 1 | 1.844 | 1.844–1.844 | 3 | 2.617 | 1.750–3.100 | N/A | 5 | 2.725 | 0.000–4.188 | 0 | N/A | N/A | N/A |
AOR | 6 | 3.781 | 3.688–4.063 | 3 | 2.567 | 1.800–3.250 | n.s. | 5 | 3.513 | 3.313–3.813 | 7 | 2.734 | 2.250–3.500 | < 0.002* |
BOS | 6 | 1.823 | 1.563–2.063 | 3 | 1.717 | 1.550–1.950 | n.s. | 5 | 1.525 | 1.188–2.000 | 7 | 1.857 | 1.500–2.063 | n.s. |
HL | 6 | 6.192 | 5.923–6.538 | 6 | 5.383 | 4.650–5.900 | < 0.005* | 5 | 5.569 | 5.308–5.846 | 7 | 4.758 | 4.308–5.615 | < 0.005* |
LOP | 6 | 5.295 | 5.000–6.000 | 6 | 4.767 | 3.950–5.400 | n.s. | 5 | 4.723 | 4.308–5.077 | 7 | 4.805 | 3.950–7.000 | n.s. |
POR | 6 | 1.281 | 1.188–1.375 | 6 | 0.942 | 0.800–1.050 | < 0.0001* | 5 | 1.15 | 1.125–1.188 | 7 | 0.929 | 0.750–1.188 | < 0.005* |
POS | 6 | 1.458 | 1.000–1.688 | 3 | 1.55 | 1.200–1.750 | n.s. | 5 | 1.425 | 0.813–1.625 | 7 | 1.307 | 1.063–1.625 | n.s. |
R1 | 6 | 2.133 | 2.000–2.250 | 6 | 1.808 | 1.650–2.000 | < 0.002 | 5 | 1.87 | 1.750–2.050 | 6 | 1.8 | 1.650–2.150 | n.s. |
R2 | 6 | 4.133 | 3.750–4.450 | 6 | 3.417 | 2.900–3.850 | < 0.002 | 5 | 3.83 | 3.750–3.950 | 6 | 3.292 | 2.950–4.000 | n.s. |
R3 | 6 | 1.202 | 1.000–1.610 | 6 | 0.967 | 0.850–1.050 | < 0.05 n.s. | 5 | 1.2 | 1.150–1.250 | 6 | 0.933 | 0.700–1.150 | < 0.01* |
S | 6 | 1.308 | 1.231–1.538 | 6 | 1.033 | 0.900–1.250 | < 0.005* | 5 | 1.169 | 1.077–1.231 | 7 | 0.95 | 0.850–1.231 | < 0.005* |
TL | 6 | 34.58 | 32.170–38.000 | 6 | 33.12 | 28.830–34.200 | n.s. | 5 | 28.73 | 26.670–30.170 | 7 | 29.98 | 23.830–35.500 | n.s. |
TS | 6 | 3.281 | 2.750–3.500 | 3 | 3.15 | 2.500–3.650 | n.s. | 5 | 2.95 | 2.750–3.188 | 7 | 3.164 | 2.750–3.688 | n.s. |
WAE | 6 | 2.487 | 2.385–2.692 | 6 | 2.492 | 2.200–2.800 | n.s. | 5 | 2.323 | 2.231–2.462 | 7 | 2.415 | 2.154–2.900 | n.s. |
WE | 6 | 0.599 | 0.500–0.625 | 6 | 0.733 | 0.600–0.900 | n.s. | 5 | 0.594 | 0.563–0.625 | 7 | 0.654 | 0.500–0.800 | n.s. |
WOP | 6 | 6.526 | 6.077–7.385 | 6 | 6.633 | 2.800–8.000 | n.s. | 5 | 6.308 | 6.231–6.385 | 7 | 5.352 | 3.100–7.385 | n.s. |
Males (mm) | Females (mm) | Holotype (mm) | |||||||
---|---|---|---|---|---|---|---|---|---|
Min. | Mean | Max. | sd | Min. | Mean | Max. | sd | ||
A1 | 1.41 | 1.538 | 1.63 | 0.086 | 1.41 | 1.63 | 1.78 | 0.138 | 1.59 |
A2 | 4.13 | 4.77 | 5.31 | 0.483 | 4.5 | 4.718 | 5.28 | 0.293 | 5.19 |
A3 | 3.69 | 4.194 | 4.47 | 0.303 | 4.22 | 4.363 | 4.53 | NA | 4.31 |
A4 | 2.75 | 2.952 | 3.19 | 0.197 | 2.75 | 3.282 | 3.5 | 0.279 | 3.13 |
AOR | 3.31 | 3.512 | 3.81 | 0.189 | 3.69 | 3.782 | 4.06 | 0.145 | 3.56 |
BOS | 1.19 | 1.526 | 2 | -0.332 | 1.56 | 1.823 | 2.06 | 0.191 | 1.5 |
HL | 5.31 | 5.57 | 5.85 | 0.261 | 5.92 | 6.193 | 6.54 | 0.217 | 5.85 |
LOP | 4.31 | 4.724 | 5.08 | 0.305 | 5 | 5.295 | 6 | 0.371 | 4.77 |
POR | 1.13 | 1.154 | 1.19 | 0.033 | 1.19 | 1.282 | 1.38 | 0.076 | 1.19 |
POS | 0.81 | 1.426 | 1.63 | -0.349 | 1 | 1.46 | 1.69 | 0.28 | 1.63 |
R1 | 1.75 | 1.87 | 2.05 | 0.130 | 2 | 2.133 | 2.25 | 0.103 | 2.05 |
R2 | 3.75 | 3.83 | 3.95 | 0.084 | 3.75 | 4.133 | 4.45 | 0.225 | 3.85 |
R3 | 1.15 | 1.2 | 1.25 | 0.05 | 1 | 1.202 | 1.61 | 0.211 | 1.25 |
S | 1.08 | 1.168 | 1.23 | 0.063 | 1.23 | 1.308 | 1.54 | 0.120 | 1.15 |
TL | 26.67 | 28.74 | 30.17 | 1.677 | 32.17 | 34.58 | 38 | 2.056 | 29.67 |
TS | 2.84 | 3.408 | 4.19 | NA | 1.84 | 1.84 | 1.84 | NA | 3.13 |
WAE | 2.23 | 2.324 | 2.46 | 0.084 | 2.38 | 2.485 | 2.69 | 0.117 | 2.31 |
WE | 0.56 | 0.592 | 0.63 | 0.025 | 0.5 | 0.602 | 0.63 | 0.052 | 0.59 |
WOP | 6.23 | 6.306 | 6.38 | 0.075 | 6.08 | 6.525 | 7.38 | 0.458 | 6.38 |
Head shape comparison between T. mopan specimens and T. dimidiata and T. gerstaeckeri revealed a unique separate cluster comprising T. mopan for both PCA and CVA (Figure
Both ML phylogenies recovered T. mopan as an independently evolving lineage, with the highest bootstrap support recovered for each phylogeny. Triatoma mopan was recovered as a sister taxon to T. dimidiata upon ITS-2 phylogenetic reconstruction and as sister to T. gerstaeckeri when cytb was used for the reconstruction (Figure
Pairwise Kimura 2-parameter genetic distances revealed T. mopan to diverge at least 2% from the other lineages when distances were calculated for ITS-2; while for cytb the minimum pairwise distance between T. mopan and the closest examined species increases to about 10% (Figure
Phylogenetic studies of the diverse T. dimidiata have long shown the taxa to be composed of at least three independently evolving lineages (
We have compared T. mopan with T. dimidiata using different systematic approaches: classic morphology, geometric morphometric and molecular phylogeny, and the results agree in that these are separate species. Diagnostic characters were observed on the pronotum, legs and abdomen and PCA and CVA results place both in separate clusters (Figures
The morphological comparison of T. mopan with the description of T. dimidiata (
Character comparison between T. mopan, T. dimidiata, and Triatoma from Lanquin cave, based on the description of
T. mopan | Triatoma Lanquin | T. dimidiata | |
---|---|---|---|
Antenna | first antennal segment attaining to the level of or surpassing the apex of clypeus | first antennal segment surpassing the apex of clypeus | first antennal segment attaining to the level of the apex of clypeus |
POR/AOR | 2.8–3.2 | 4 | 2.5–3 |
Ratio antennae segments | 1:2.7–3.4:2.5-2.6:1.15 | 1:2.5:2.2:2.3 | 1:3.2–3.8:2.5:2.2. |
Eyes | surpassing the level of the ventral surface of the head | not surpassing the level of the ventral surface of the head | attaining to the level of the ventral surface of the head |
The geometric morphometric comparison of the head shape (PCA and CVA) also placed the Lanquin specimens closer to T. dimidiata (but separate from) than to T. mopan, which forms a unique separate cluster (Figure
The comparison of the morphology of T. mopan with T. dimidiata shows a clear trend in cave adaptation evolution. Besides the diminished overal pigmentation of the specimens, T. mopan exhibits much denser sensillae on the visible labial segments (Figure
In combination, the morphological characters with molecular phylogeney and geometric morphometry of the head show that T. mopan is an independently evolving lineage, separate from T. dimidiata. The comparison with the types of T. dimidiata maculipennis, T. dimidiata capitata and the description given by
We are grateful for prior work by Heather Axen, Bethany Richards, Nicholas de la Rúa, and Dulce Bustamante that suggested T. mopan was a separate species. We also thank Leticia Nery and Renata Cardoso, from the Laboratório de Biodiversidade Entomológica, Instituto Oswaldo Cruz, FIOCRUZ for help with the collection specimens used in this study; Lisa Chamberland for the help with the photos; Dr. Jurgern Deckert and Bernhard Schurian from the Museum für Naturkunde Berlin for the photos of the types of T. dimidiata maculipennis; and Rachel Diaz-Bastin from the California Academy of Sciences for the photos of the type of T. dimidiata capitata. We also thank Thomas Henry, curator of the Heteroptera collection at the National Museum of Natural History, Smithsonian Institution for the invaluable comments on this manuscript.
Funding was provided by grant R03AI26268/1-2 from the National Institute of Allergy and Infectious Diseases (NIAID) at the National Institutes of Health (NIH); the National Science Foundation (NSF) grant BCS-1216193 as part of the joint NSF-NIH-USDA (United States Department of Agriculture) Ecology and Evolution of Infectious Diseases program; and CNPq Research Productivity grant 305055/2016-0. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the funding organizations.
T. mopan × T. dimidiata - boxplots comparing the characters.
T. mopan description - R codes.