New and Common Haplotypes Shape Genetic Diversity in Asian Tiger Mosquito Populations from Costa Rica and Panamaby K. Futami, A. Valderrama, M. Baldi, N. Minakawa, R. Marin Rodriguez, L. F. Chaves

Journal of Economic Entomology


Insect Science / Ecology


Foods Eaten by Some Bats from Costa Rica and Panama

J. O. Whitaker, J. S. Findley

The Costa Rica-Panama Boundary Dispute

Chandler P. Anderson

Some new hysteriaceous Fungi from Costa Rica

J. Checa, R.A. Shoemaker, L. Umana

Rudgea monofructus (Rubiaceae), an Unusual New Species from Costa Rica

Charlotte M. Taylor, Jorge Gómez-Laurito, John Dwyer, Jorge Gomez-Laurito



New and Common Haplotypes Shape Genetic Diversity in Asian

Tiger Mosquito Populations from Costa Rica and Panama´


L. F. CHAVES,1,3,5

J. Econ. Entomol. 1–8 (2015); DOI: 10.1093/jee/tou028

ABSTRACT The Asian tiger mosquito, Aedes albopictus (Skuse) (Diptera: Culicidae), is a vector of several human pathogens. Ae. albopictus is also an invasive species that, over recent years, has expanded its range out of its native Asia. Ae. albopictus was suspected to be present in Central America since the 1990s, and its presence was confirmed by most Central American nations by 2010. Recently, this species has been regularly found, yet in low numbers, in limited areas of Panama´ and Costa Rica (CR). Here, we report that short sequences (558 bp) of the mitochondrial cytochrome oxidase subunit 1 (COI) and

NADH dehydrogenase subunit 5 genes of Ae. albopictus, had no haplotype diversity. Instead, there was a common haplotype for each gene in both CR and Panama´. In contrast, a long COI sequence (1,390 bp) revealed that haplotype diversity (6SD) was relatively high in CR (0.726 0.04) when compared with

Panama´ (0.336 0.13), below the global estimate for reported samples (0.896 0.01). The long COI sequence allowed us to identify seven (five new) haplotypes in CR and two (one new) in Panama´.

A haplotype network for the long COI gene sequence showed that samples from CR and Panama´ belong to a single large group. The long COI gene sequences suggest that haplotypes in Panama´ and CR, although similar to each other, had a significant geographic differentiation (Kst¼ 1.33; P< 0.001). Thus, most of our results suggest a recent range expansion in CR and Panama´.

KEY WORDS mitochodrial COI, ND5, Aedes albopictus, invasive species, dengue vectors


The Asian tiger mosquito, Aedes albopictus (Skuse) (Diptera: Culicidae), is an invasive insect species that has been expanding globally in the past 150 yr (Lounibos 2002, Benedict et al. 2007, Bonizzoni et al. 2013). Its successful expansion is mainly because of its desiccation-tolerant eggs and adaptation to small aquatic habitats (Lambrechts et al. 2010). These characteristics allowed Ae. albopictus to inhabit artificial water containers that promote its close interaction with humans (Bonizzoni et al. 2013). Moreover, Ae. albopictus aggressive biting behavior (Ponlawat and Harrington 2005) and vectorial competence, allow its females to transmit a wide array of arboviruses (Benedict et al. 2007, Paupy et al. 2009), most notoriously dengue virus (Lambrechts et al. 2010) and Chikungunya virus (Paupy et al. 2009). Moreover, for dengue virus, mosquitoes can get infected vertically, i.e., without involving vertebrate hosts (Martins et al. 2012).

Several studies have suggested the geographical origin of Ae. albopictus to be in Southeast Asia (Hawley et al. 1987, Khambhampati et al. 1991, Rai 1991, Porretta et al. 2012) from where it likely invaded, mainly by means of maritime trade, most of East Asia before the end of the 19th century (Lounibos 2002). Nevertheless, Ae. albopictus gained notoriety in the 1980s, after becoming established in Harris County, TX, where it became a dominant vector species in the Houston area (Sprenger and Wuithiranyagool 1986). Subsequent molecular genetics studies, and additional ecological evidence, suggested Japan as the likely place for the origin of this infestation (Hawley et al. 1987,

Khambhampati et al. 1991, Rai 1991, Lounibos 2002,

Bonizzoni et al. 2013). The detection of the Asian tiger mosquito in United States was not a mere description of a range expansion, it highlighted how the expansion and establishment of this species, like many other invasive species, has been driven by the intensification of global commodity trade (Bonizzoni et al. 2013), first by its detection at seaports (Eads 1972) and its subsequent detection and establishment at the final destination of trade commodities (Reiter and Darsie 1984, Sprenger and Wuithiranyagool 1986). For example, Ae. albopictus was already present in Albania in the late 1970s, a time when Albania was the main European commercial partner of China, a country within the native range of Ae. albopictus (Adhami 1 Department of Vector Ecology and Environment, Institute of

Tropical Medicine (NEKKEN), Nagasaki University, 852-8523, Sakamoto 1-12-4, Nagasaki, Japan. 2 Departamento de Entomologı´a Me´dica, Instituto Conmemorativo

Gorgas de Estudios de la Salud (ICGES), Ministerio de Salud, Ciudad de Panama´, Repu´blica de Panama´. 3 Programa de Investigacio´n en Enfermedades Tropicales (PIET),

Escuela de Medicina Veterinaria, Universidad Nacional, Heredia,

Costa Rica. 4 Departamento de Control de Vectores, Ministerio de Salud, San

Jose´, Costa Rica. 5 Corresponding author, e-mail:

VC The Authors 2015. Published by Oxford University Press on behalf of Entomological Society of America.

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Journal of Economic Entomology Advance Access published January 30, 2015 and Reiter 1998). Similarly, in the mid-1980s, the species was detected in Sa˜o Paulo, Brazil (Forattini 1986), the economic heart of South America. Currently, Ae. albopictus has spread over Europe, Oceania, and reports of its presence and establishment all over Africa are becoming increasingly common, with extensive documentation of trade playing a major role on Ae. albopictus expansion (Bonizzoni et al. 2013).

In the New World, Ae. albopictus spread to Mexico by the early 1990s (Rai 1991, Lounibos 2002) was suspected in most Central American countries by the late 1990s (Eritja et al. 2005), with all countries confirming its presence by 2010 (Bonizzoni et al. 2013).

In Panama´, Ae. albopictus was first detected in 2002, in the “24 de diciembre” neighborhood of Panama´ city (ICGES 2003). According to dengue entomological surveys from Panama´’s Ministry of Health, Ae. albopictus has been mainly found in urban settings (Espino et al. 2011, Dı´az 2012). Nevertheless, from 2002, Ae. albopictus has been monotonically increasing its abundance, having a house index close to 0.5 % in 2013 (Dı´az 2012). In Costa Rica (CR), Ae. albopictus larvae were first recorded during 2007 in coconut shells at