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Genetic Diversity and Population Structure of Busseola Segeta Bowden (Lepidoptera; Noctuidae): a Case Study of Host Use Diversif

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Genetic Diversity and Population Structure of Busseola Segeta Bowden (Lepidoptera; Noctuidae): a Case Study of Host Use Diversif Insects 2012, 3, 1156-1170; doi:10.3390/insects3041156 OPEN ACCESS insects ISSN 2075-4450 www.mdpi.com/journal/insects/ Article Genetic Diversity and Population Structure of Busseola segeta Bowden (Lepidoptera; Noctuidae): A Case Study of Host Use Diversification in Guineo-Congolian Rainforest Relic Area, Kenya *HRUJH22QJ¶DPR 1,*, Bruno P. Le Ru 2,3, Pascal Campagne 3, Antoine Branca 4, Paul-Andre Calatayud 2,3, Claire Capdevielle-Dulac 4 and Jean-Francois Silvain 4 1 School of Biological Science, College of Physical and Biological Sciences (Chiromo Campus), University of Nairobi, Nairobi 30197, Kenya 2 Unité de Recherche IRD 072, International Centre of Insect Physiology and Ecology (ICIPE), Nairobi 30772, Kenya; E-Mails: [email protected] (B.P.L.R.); [email protected] (P.-A.C.) 3 Unité de Recherche IRD 072, International Centre of Insect Physiology and Ecology (ICIPE), Université Paris-Sud 11, Orsay cedex 91405, France; E-Mails: [email protected] 4 Unité de Recherche IRD 072, CNRS, Laboratoire Evolution, Génomes et spéciation, UPR 9034, 91198 Gif-sur-Yvette cedex, France et Université Paris-Sud 11, Orsay cedex 91405, France; E-Mails: [email protected] (A.B.); [email protected] (C.C.-D.); [email protected] (J.-F.S.) * Author to whom correspondence should be addressed; E-Mail: [email protected]. Received: 27 July 2012; in revised form: 22 August 2012 / Accepted: 30 August 2012 / Published: 6 November 2012 Abstract: Habitat modification and fragmentation are considered as some of the factors that drive organism distribution and host use diversification. Indigenous African stem borer pests are thought to have diversified their host ranges to include maize [Zea mays L.] and sorghum [Sorghum bicolor (L.) Moench] in response to their increased availability through extensive cultivation. However, management efforts have been geared towards reducing pest populations in the cultivated fields with few attempts to understand possible evolution of "new" pest species. Recovery and growing persistence of Busseola segeta Bowden on maize (Zea mays L.) in Kakamega called for studies on the role of wild host plants on the invasion of crops by wild borer species. A two-year survey was carried out in a small agricultural landscape along the edge of Kakamega forest (Kenya) to assess host range and population genetic structure of B. segeta. The larvae of B. segeta were found on nine different plant species with the majority occurring on maize and sorghum. Of forty Insects 2012, 3 1157 cytochrome b haplotypes identified, twenty-three occurred in both wild and cultivated habitats. The moths appear to fly long distances across the habitats with genetic analyses revealing weak differentiation between hosts in different habitats (FST = 0.016; p = 0.015). However, there was strong evidence of variation in genetic composition between growing seasons in the wild habitat (FST = 0.060; p < 0.001) with emergence or disappearance of haplotypes between habitats. Busseola segeta is an example of a phytophagous insect that utilizes plants with a human induced distribution range, maize, but does not show evidence of host race formation or reduction of gene flow among populations using different hosts. However, B. segeta is capable of becoming an important pest in the area and the current low densities may be attributed to the general low infestation levels and presence of a wide range of alternative hosts in the area. Keywords: Cytochrome b; exchange; growing seasons; haplotypes; wild habitat; Zea mays 1. Introduction Natural ecosystems provide important habitats for a wide range of organisms. Unfortunately, these habitats have been subjected to diverse forms of modifications over the past half century resulting in significant loss and fragmentation of natural ecosystems [1±4]. Organisms exposed to these modifications, particularly phytophagous insects, exhibit a wide range of responses varying from host range expansion to local species extinction [5±8]. The ability of insects to utilize different host plants has been suggested to be a dynamic and transient phase [9]. During or after this phase, species can shift to novel host plants or re-specialize on ancestral ones. Expanding the range of host plants might also be a factor leading to higher net speciation rates. Lepidopteran stem borers are among the phytophagous insects that expanded their host ranges upon exposure to anthropogenic changes. In East Africa, stem borer pests, Busseola fusca Fuller and Sesamia calamistis Hampson, are examples of phytophagous insects that expanded their hosts and eventually specialised to feed on maize and sorghum where they remain important pests [10]. Though trade-offs associated with host use diversification have been evaluated in different contexts and applied in stem borer pest management (e.g., in the "Push-Pull" system, [11]), this study focused on the effects of fine scale host use diversification on genetic structure of a native phytophagous stem borer sub-species, Busseola segeta Bowden, and potential influence of natural habitats on its dynamics. Busseola segeta was for a long time known to infest wild Poaceae plants in Kenya [12] until 2005 when it was first reported on maize [Zea mays L.] in Kakamega and Kisii [13]. During the first recovery, authors thought that B. segeta eggs may have been accidentally oviposited by gravid moths from wild hosts growing in the adjacent forests. Since then, this species has persisted in maize and sorghum [Sorghum bicolor (L.) Moench] fields in Kakamega, where sometimes its population exceeds B. fusca - the native dominant pest species [14]. Despite this growing importance, B. segeta infests a wide range of non-cereal graminaceous plants in the vicinity, making it the only native stem borer species found in both wild and cultivated fields in this area [15]. Host use diversification remains important to agricultural entomologists as it may mark the beginning of an evolutionary process that Insects 2012, 3 1158 would result in a new pest. In addition to evolution of a new pest, host use diversification may sometimes result in adaptation to local conditions, or reduction in gene flow among populations using different hosts [16,17]. In this context, the source-sink role of cultivated and natural habitats in the life cycle and genetic composition of B. segeta has not been studied. Consequently, potential host use specialization and the reciprocal influence of populations from different habitats through exchange of individuals/genes are not known. The study of dispersal processes is a central problem in ecology, population genetics and conservation. For this reason, the estimation of dispersal rates has been one of the most investigated problems in population biology. Dispersal parameters can be directly estimated using ecological approaches such as mark-release-recapture methods but might not be applicable in studies involving sampling the propagules. In these cases, population genetics approaches provide a better alternative because the information contained in DNA can provide gene flow parameter estimates for different and complementary timescales [18,19]. Among molecular markers, mitochondrial markers, particularly the cytochrome b (Cyt. b) gene, has been applied in both phylogeographic studies [20] and estimation of long-standing historical host use differentiation [21]. In this study, the Cyt. b gene was used to examine host use diversification among B. segeta moths collected in the agricultural landscape along the Kakamega forest. 2. Experimental 2.1. Description of the Study Area Kakamega Forest is located in western Kenya about 40 km North West of Lake Victoria. It is the only remnant of Guineo-Congolian rainforest in Kenya and was gazetted in 1933 by the Forest Department to enhance its protection [22±24]. Despite the conservation measures, high human population density in the area (175 individuals/km2) has led to considerable long-term human influence on the forest and its environs [24]. The area is generally suitable for rain fed agriculture (temperature ranges from 12.7 °C to 27.1 °C and average rainfall is 1,650 mm), and parts of the forest have been excised for establishment of crop fields as demand for agricultural land increases. Surveyed landscape, 21.2 km2 along the forest edge, was originally part of the main forest block but was opened for cultivation of maize and sorghum due to human population pressure [23]. It is thus characterised by cultivated fields interspersed with uncultivated areas. The cultivated areas are covered by small farms, usually less than 2 ha, where maize, sorghum, finger millet and sugarcane are grown for domestic consumption. The uncultivated areas are covered by homes, forest edges and rivers. The natural habitats²hereafter referred to as wild habitats²support a wide range of plant species, some of which are potential hosts of stem borers [25]. The majority of the wild plants here that are considered as potential hosts of stem borers grow along the edge of the forest, around crop fields, and along the river banks. The area experiences a bimodal rainfall, which allows for two cropping seasons. The first season lasts from March to mid-July (long rain growing season, LR) and the second from mid-August to November (short rain growing season, SR). The area experiences light rain from the beginning of December to the end of February, hereafter referred to as non-cropping season. Insects 2012, 3 1159 2.2. Sampling, Rearing and Identification of Stem Borers Surveys were carried out in both wild and cultivated habitats in 2005±2007 growing seasons (SR, 2005 & 2006; LR, 2006 & 2007). A total of 32 maize fields were identified and surveyed for stem borer infestation during each sampling session. In each field, 100 maize plants were randomly selected and inspected for stem borer infestation symptoms five weeks after germination. During field sampling, only infested stems were dissected for larval recovery. Since stem borer infestations are usually low in wild habitats [13,26], we adopted two sampling approaches during each sampling session.
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