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Genitalic Differentiations in Neoleucinodes Elegantalis (Gueneé) (Lepidoptera: Crambidae) Associated with Solanaceae Crops in Ecuador

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Genitalic Differentiations in Neoleucinodes Elegantalis (Gueneé) (Lepidoptera: Crambidae) Associated with Solanaceae Crops in Ecuador insects Article Genitalic Differentiations in Neoleucinodes elegantalis (Gueneé) (Lepidoptera: Crambidae) Associated with Solanaceae Crops in Ecuador Michelle Noboa 1, William Viera 1,* ID , Ana Díaz 2, Wilson Vásquez 3 and Lenin Ron 1,4 1 Instituto Nacional de Investigaciones Agropecuarias (INIAP), Programa Nacional de Fruticultura, Tumbaco, Quito 170184, Ecuador; [email protected] (M.N.); [email protected] (L.R.) 2 Corporación Colombiana de Investigación Agropecuaria (CORPOICA), Centro de Investigación Obonuco, Km 5, Vía Pasto, Pasto 520038, Colombia; [email protected] 3 Facultad de Ingeniería y Ciencias Agropeuarias, Universidad de las Américas (UDLA), José Queri, Quito 170137, Ecuador; [email protected] 4 Facultad de Medicina Veterinaria y Zootecnia, Centro Internacional de Zoonosis. Universidad Central del Ecuador, Quito 170521, Ecuador * Correspondence: [email protected]; Tel.: +593-022-371-057 Academic Editors: Michael J. Stout, Jeff Davis, Rodrigo Diaz and Julien M. Beuzelin Received: 12 July 2017; Accepted: 25 August 2017; Published: 31 August 2017 Abstract: Neoleucinodes elegantalis (Guenée) is an oligophagous species of plants in the Solanaceae family that has a broad geographical distribution in the tropical zones of South America. It is the most important insect pest of naranjilla (Solanum quitoense Lamarck), a crop grown in threatened areas of the tropical old-growth forest in Ecuador. In this study, two host-specific populations of N. elegantalis were collected from infested fruit of naranjilla and tree tomato (Solanum betaceum Cavanilles) in different locations. Sexually virgin adult insects (93 females and 103 males) were dissected to extract their genitalia to measure 12 morphological variables in females and six in males, resulting in six and four informative variables respectively. Using univariate and multivariate analysis of variance, it was found that the Solanaceous host was the main factor differentiating the area measurements of the seventh abdominal segment and ostium bursae in female genitalia, and cornuti length in male genitalia. Principal components generated with these measurements were employed in a logistic regression model for the classification of the Solanaceous host. Female genitalia of individuals from S. betaceum showed significantly larger ostium bursae relative to female genitalia from S. quitoense. For males, individuals collected from S. betaceum showed longer cornuti length than samples collected from S. quitoense. The results suggest genotypic differentiation according to the Solanaceous host or phenotypic plasticity in N. elegantalis. Further molecular and bio-geographical studies are needed to properly differentiate N. elegantalis populations that would help in the control of this pest. Keywords: genitalia; morphometry; moth; Solanaceae; subspecies 1. Introduction Recent studies on the biology of the fruit borer Neoleucinodes elegantalis (Guenée, 1984) (Lepidoptera: Crambidae) carried out in Latin America, have found that this pest is an oligophagous species of plants in the Solanaceae family, and is distributed in almost all countries of South America infesting various crops of economic importance, such as S. lycopersicum (tomato), S. betaceum (tree tomato), S. capsicum (pepper), and S. quitoense (naranjilla) [1–4]. According to Capps (1948), this species has the following characters: a simple antenna; slightly annulate; labial palpus upturned; remarkably shorter maxillary palpus in males than in females; Insects 2017, 8, 91; doi:10.3390/insects8030091 www.mdpi.com/journal/insects Insects 2017, 8, 91 2 of 11 Insects 2017, 8, 91 2 of 11 frons evenly rounded; a posterodorsal area of the head with white scales predominant; a dark fuscous evenly rounded; a posterodorsal area of the head with white scales predominant; a dark fuscous brownbrown thorax thorax (dorsal (dorsal view) view) that that is is white white inin ventralventral view; an an abdomen abdomen with with a aconspicuous conspicuous white white band band composedcomposed of of all all the the first first and and variable variable portions portions ofof the second a a third third segments; segments; white white hyalinate hyalinate wings wings withwith conspicuous conspicuous squamous squamous areas areas of of cinnamon cinnamon brownbrown [[5],5], as shown in in Figure Figure 1.1. Figure 1. Adults of N. elegantalis; (A) male; (B) female; (C) labial palpus of male adult; and (D) labial Figure 1. Adults of N. elegantalis;(A) male; (B) female; (C) labial palpus of male adult; and (D) labial palpus of female adult. palpus of female adult. In Ecuador, this pest is present in all the regions where naranjilla (S. quitoense) is grown. The fruitIn Ecuador,borer directly this pestaffects is presentthe fruit in pulp all the by regions boring whereand feeding naranjilla on the (S. quitoensefruit mesocarp,) is grown. producing The fruit borergalleries directly inside affects the thedeveloping fruit pulp berri by boringes [4] resulting and feeding in significant on the fruit losses mesocarp, in production producing and galleries fruit insidequality. the developing berries [4] resulting in significant losses in production and fruit quality. N.N. elegantalis elegantalisis is endemic endemic in in tropical tropical rainforestrainforest regions of of Ecuador, Ecuador, specifically specifically in in the the Andean Andean foothillsfoothills where where fruit fruit of of native native SolanaceaeSolanaceae species species su suchch as asnaranjilla naranjilla and and tree tree tomato tomato can be can found. be found. In Infact, nearly nearly 100% 100% of of naranjilla naranjilla is is grown grown in in these these areas. areas. Therefore, Therefore, farmers farmers are are obligated obligated to toapply apply insecticidesinsecticides on on the the fruit, fruit, and and in manyin many cases cases to lookto look for for new new places places in old-growthin old-growth forest forest to relocateto relocate their orchards.their orchards. As a result, As a serious result, damageserious todamage this ecosystem to this ecosystem is created is because created of because agricultural of agricultural activities. activities.There is evidence that N. elegantalis has a dichotomous behavior with respect to the preference of host species;There itis canevidence choose that one N. or elegantalis the other has but a notdichotomous both [6]. Studiesbehavior in with Colombia respect have to the identified preference four of host species; it can choose one or the other but not both [6]. Studies in Colombia have identified biotypes of N. elegantalis, correlated with different Solanaceae hosts. Those biotypes were separated by four biotypes of N. elegantalis, correlated with different Solanaceae hosts. Those biotypes were the localization in the Eastern and the Western Colombian Andes [6]. Consequently, we hypothesize separated by the localization in the Eastern and the Western Colombian Andes [6]. Consequently, we that different biotypes of N. elegantalis exist in Ecuador due to host specificity in different ecological hypothesize that different biotypes of N. elegantalis exist in Ecuador due to host specificity in different areas, due to sympatric and/or allopatric separation of this species. Thus, the present study aims to ecological areas, due to sympatric and/or allopatric separation of this species. Thus, the present study evaluate the possibility of different biotypes of N. elegantalis in Ecuador, using genitalia morphometric aims to evaluate the possibility of different biotypes of N. elegantalis in Ecuador, using genitalia measuresmorphometric of virgin measures adult specimens of virgin adult of N. elegantalisspecimens foundof N. elegantalis in two Solanaceae found in fruittwo Solanaceae crops, S. quitoense fruit andcrops,S. betaceum S. quitoense, collected and S. frombetaceum different, collected areas from of Ecuador. different areas of Ecuador. Insects 2017, 8, 91 3 of 11 2. Material and Methods 2.1. Sample Collection and Preparation Infested fruits of S. quitoense from commercial orchards and S. betaceum from abandoned orchards that were close to S. quitoense orchards were collected with larvae inside and were sent to the Entomology laboratory in INIAP-Tumbaco. We analyzed 196 N. elegantalis (103 males, 93 females) collected from different S. quitoense and S. betaceum crop areas located in the Eastern and Western foothills of the Ecuadorian Andean rainforest and were analyzed to identify potential morphological intraspecific differences. Genitalia were used because such characters are much more conserved than external characters, and because they are insignificantly influenced by environmental factors [7,8]. Infected fruits were placed in growth chambers with controlled environmental conditions (temperature 22 ± 1 ◦C, 55% relative humidity and a photoperiod of 12 h of light and 12 h of darkness) to complete their larval, pupal and adult development. N. elegantalis were collected from eight localities in five provinces of Ecuador (Table1). Both S. quitoense and S. betaceum were found together only in Los Bancos, Pichincha, and in El Chaco, Napo; in all other localities, N. elegantalis was found only on S. quitoense (Table1). Table 1. Sampling areas of the study in Ecuador, South America. Number of Specimens Locality Province Zone Altitude Host Plant (Masl) Female Male Western S. quitoense 11 10 Los Bancos Pichincha 681 Andes S. betaceum 8 16 Eastern Rio Negro Tungurahua 1242 S. quitoense 4 6 Andes S. quitoense 8 7 El Chaco Eastern
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