Jean-François Silvain

Multilocus Genetic Analysis of Host Use, Introgression, and Speciation in Host Strains of Fall Armyworm (Lepidoptera: Noctuidae)

Abstract Two genetically differentiated forms of fall armyworm, Spodoptera frugiperda (J. E. Smith), use different graminaceous host plants, coexist sympatrically throughout their ranges, yet seem to hybridize. To address the taxonomic status of the two forms, determine extent and directionality of hybridization, and examine host specificity, we compiled multilocus genotypes consisting of mitochondrial DNA (mtDNA) haplotypes, an esterase locus, and eight amplified fragment-length polymorphism (AFLP) loci in moths collected across a broad geographic range. Multilocus analyses indicated 16% of individuals sampled were potentially hybrids with a minority being F1 in origin. Analysis of host use indicated asymmetries in host specificity with one strain specific to corn, Zea mays L., and the other strain predominating on pasture grasses and rice, but occasionally using corn. Location of hybrids in nature was biased toward cornfields, the habitat used by both strains. To assess genetic divergence of each gene, we calculated their relative strain discriminating ability. Eight AFLP loci collectively had the greatest discriminating power (98%), followed by a single AFLP locus (93%) and mtDNA (91%). Esterase exhibited 89% discrimination. Esterase is X-linked along with an assortative mating trait, suggesting esterase differentiation may be maintained by association with strain-specific fitness genes. Despite strong discrimination of these genes, most of the genome surveyed was not distinct. Cytonuclear comparisons provided evidence for unidirectional matings consistent with mate preference studies. Collectively, these data support introgressive hybridization between recently evolved species that are not completely reproductively isolated. Genetic divergence in the presence of gene flow may be a common phase in the speciation process, especially in taxa whose ranges have been altered dramatically by humans.

Genetic bottleneck in invasive species: the potato tuber moth adds to the list

The level of genetic diversity within populations of introduced species has received increasing attention as an important factor influencing their survival and adaptive potential. We examined this issue with the Guatemalan potato tuber moth Tecia solanivora, an agricultural pest which has successfully invaded South America and the Canary Islands within the last 20xa0years. To analyse changes in T.xa0solanivora genetic diversity, the mitochondrial marker cytochrome b was sequenced from individuals collected across its known distribution area. High haplotypic diversity was observed in Guatemala, whereas only three haplotypes have been found in Venezuela and a single one in the remaining invaded South American countries and the Canary Islands. Invasive haplotypes were not observed in our samples from Guatemala but are closely related to Guatemalan haplotypes. These results are consistent with the hypotheses that (i) either a few individuals were introduced into Venezuela leading to a strong initial genetic bottleneck, or selection pressure may have lead to the disparition of all but a reduced number of introduced haplotypes, (ii) a second bottleneck occured between Venezuela and Colombia, and (iii) the invasion of the Canary Islands originated from South America. We further reviewed the recent literature to compare this change in genetic diversity with those reported for other invasive species. We quantified the changes in genetic diversity between native and introduced ranges for 57 biological invasions. We found that the genetic homogenization in T.xa0solanivora was among the strongest reported and discuss factors that can explain the success of invasive populations with low genetic diversity.

Temperature as a key driver of ecological sorting among invasive pest species in the tropical Andes.

Invasive species are a major threat to the sustainable provision of ecosystem products and services, both in natural and agricultural ecosystems. To understand the spatial arrangement of species successively introduced into the same ecosystem, we examined the tolerance to temperature and analyzed the field distribution of three potato tuber moths (PTM, Lepidoptera: Gelechiidae), that were introduced in Ecuador since the 1980s. We studied physiological responses to constant temperatures of the three PTM species under laboratory conditions and modeled consequences for their overall population dynamics. We then compared our predictions to field abundances of PTM adults collected in 42 sites throughout central Ecuador. Results showed that the three PTM species differed with respect to their physiological response to temperature. Symmetrischema tangolias was more cold tolerant while Tecia solanivora had the highest growth rates at warmer temperatures. Phthorimaea operculella showed the poorest physiological performance across the range of tested temperatures. Overall, field distributions agree with predictions based on physiological experiments and life table analyses. At elevations >3000 m, the most cold-tolerant species, S. tangolias, was typically dominant and often the only species present. This species may therefore represent a biological sensor of climate change. At low elevations (<2700 m), T. solanivora was generally the most abundant species, probably due to its high fecundity at high temperatures. At mid elevations, the three species co-occurred, but P. operculella was generally the least abundant species. Consistent with these qualitative results, significant regression analyses found that the best predictors of field abundance were temperature and a species x temperature interaction term. Our results suggest that the climatic diversity in agricultural landscapes can directly affect the community composition following sequential invasions. In the tropical Andes, as in other mountain ecosystems, the wide range of thermal environments found along elevational gradients may be one reason why the risks of invasion by successively introduced pest species could increase in the near future. More data on potential biological risks associated with climatic warming trends in mountain systems are therefore urgently needed, especially in developing nations where such studies are lacking.

Community-Based Participatory Research Helps Farmers and Scientists to Manage Invasive Pests in the Ecuadorian Andes

Participatory research has not been a conspicuous methodology in developing nations for studying invasive pests, an increasing threat to the sustainable development in the tropics. Our study presents a community-based monitoring system that focuses on three invasive potato tuber moth species (PTM). The monitoring was developed and implemented by young farmers in a remote mountainous area of Ecuador. Local participants collected data from the PTM invasion front, which revealed clear connection between the abundance of one of the species (Tecia solanivora) and the remoteness to the main market place. This suggests that mechanisms structuring invasive populations at the invasion front are different from those occurring in areas invaded for longer period. Participatory monitoring with local people may serve as a cost-effective early warning system to detect and control incipient invasive pest species in countries where the daily management of biological resources is largely in the hands of poor rural people.

Disentangling dispersal, vicariance and adaptive radiation patterns: a case study using armyworms in the pest genus Spodoptera (Lepidoptera: Noctuidae).

Thanks to the recent development of integrative approaches that combine dated phylogenies with models of biogeographic evolution, it is becoming more feasible to assess the roles of dispersal and vicariance in creating complex patterns of geographical distribution. However, the historical biogeography of taxa with good dispersal abilities, like birds or flying insects, still remains largely unknown because of the lack of complete phylogenies accompanied by robust estimates of divergence times. In this study, we investigate the evolution and historical biogeography of the globally distributed pest genus Spodoptera (Lepidoptera: Noctuidae) using complete taxon sampling and an extensive set of analyses. Through the analysis of a combined morphological and molecular dataset, we provide the first robust phylogenetic framework for this widespread and economically important group of moths. Historical biogeography approaches indicate that dispersal events have been the driving force in the biogeographic history of the group. One of the most interesting findings of this study is the probable occurrence of two symmetric long-distance dispersal events between the Afrotropical and the Neotropical region, which appear to have occurred in the late Miocene. Even more remarkably, our dated phylogenies reveal that the diversification of the clade that includes specialist grass feeders has followed closely the expansion of grasslands in the Miocene, similar to the adaptive radiation of specialist grazing mammals during the same period.

Importance of plant physical cues in host acceptance for oviposition by Busseola fusca

Plant and surrogate stems exhibiting specific combinations of physical cues were used to determine which plant‐related stimuli influence the oviposition of Busseola fusca (Fuller) (Lepidoptera: Noctuidae). The number of eggs and egg batches laid per female increased with an increase in diameter of both natural and artificial stems. Direct observations of the oviposition behaviour (walking, antennating, and sweeping with the ovipositor) indicated that the female moths preferred oviposition supports with a large diameter and non‐pubescent or smooth surfaces over pubescent or rough ones. Pubescence and rough surfaces significantly affected the behavioural steps leading to oviposition by interfering with the ovipositor sweep process necessary to find a suitable oviposition site. Furthermore, more eggs and egg batches were laid on soft than rigid supports. The rigidity of the support affected the proper insertion of the ovipositor for egg deposition. Our results underline the importance of physical stimuli in B. fuscas choice of an oviposition site, which may facilitate the identification of potential host plants or preferred oviposition sites on a plant for this species.

Native Prey and Invasive Predator Patterns of Foraging Activity: The Case of the Yellow-Legged Hornet Predation at European Honeybee Hives

Contrary to native predators, which have co-evolved with their prey, alien predators often benefit from native prey naïveté. Vespa velutina, a honeybee predator originating from Eastern China, was introduced into France just before 2004. The present study, based on video recordings of two beehives at an early stage of the invasion process, intends to analyse the alien hornet hunting behaviour on the native prey, Apis mellifera, and to understand the interaction between the activity of the predator and the prey during the day and the season. Chasing hornets spent most of their time hovering facing the hive, to catch flying honeybees returning to the hive. The predation pressure increased during the season confirming previous study based on predator trapping. The number of honeybee captures showed a maximum peak for an intermediate number of V. velutina, unrelated to honeybee activity, suggesting the occurrence of competition between hornets. The number of honeybees caught increased during midday hours while the number of hornets did not vary, suggesting an increase in their efficacy. These results suggest that the impact of V. velutina on honeybees is limited by its own biology and behaviour and did not match the pattern of activity of its prey. Also, it could have been advantageous during the invasion, limiting resource depletion and thus favouring colonisation. This lack of synchronization may also be beneficial for honeybee colonies by giving them an opportunity to increase their activity when the hornets are less effective.

Phylogenetic Molecular Species Delimitations Unravel Potential New Species in the Pest Genus Spodoptera Guenée, 1852 (Lepidoptera, Noctuidae)

Nowadays molecular species delimitation methods promote the identification of species boundaries within complex taxonomic groups by adopting innovative species concepts and theories (e.g. branching patterns, coalescence). As some of them can efficiently deal with large single-locus datasets, they could speed up the process of species discovery compared to more time consuming molecular methods, and benefit from the existence of large public datasets; these methods can also particularly favour scientific research and actions dealing with threatened or economically important taxa. In this study we aim to investigate and clarify the status of economically important moths species belonging to the genus Spodoptera (Lepidoptera, Noctuidae), a complex group in which previous phylogenetic analyses and integrative approaches already suggested the possible occurrence of cryptic species and taxonomic ambiguities. In this work, the effectiveness of innovative (and faster) species delimitation approaches to infer putative species boundaries has been successfully tested in Spodoptera, by processing the most comprehensive dataset (in terms of number of species and specimens) ever achieved; results are congruent and reliable, irrespective of the set of parameters and phylogenetic models applied. Our analyses confirm the existence of three potential new species clusters (for S. exigua (Hübner, 1808), S. frugiperda (J.E. Smith, 1797) and S. mauritia (Boisduval, 1833)) and support the synonymy of S. marima (Schaus, 1904) with S. ornithogalli (Guenée, 1852). They also highlight the ambiguity of the status of S. cosmiodes (Walker, 1858) and S. descoinsi Lalanne-Cassou & Silvain, 1994. This case study highlights the interest of molecular species delimitation methods as valuable tools for species discovery and to emphasize taxonomic ambiguities.

Modeling invasive species spread in complex landscapes: the case of potato moth in Ecuador

Tropical mountains have a long history of human occupation, and although vulnerable to biological invasions, have received minimal attention in the literature. Understanding invasive pest dynamics in socio-ecological, agricultural landscapes, like the tropical Andes, is a challenging but timely issue for ecologists as it may provide developing countries with new tools to face increasing threats posed by these organisms. In this work, road rehabilitation into a remote valley of the Ecuadorian Andes constituted a natural experiment to study the spatial propagation of an invasive potato tuber moth into a previously non-infested agricultural landscape. We used a cellular automaton to model moth spatio-temporal dynamics. Integrating real-world variables in the model allowed us to examine the relative influence of environmental versus social landscape heterogeneity on moth propagation. We focused on two types of anthropogenic activities: (1) the presence and spatial distribution of traditional crop storage structures that modify local microclimate, and (2) long-distance dispersal (LDD) of moths by human-induced transportation. Data from participatory monitoring of pest invasion into the valley and from a larger-scale field survey on the Ecuadorian Andes allowed us to validate our model against actual presence/absence records. Our simulations revealed that high density and a clumped distribution of storage structures had a positive effect on moth invasion by modifying the temperature of the landscape, and that passive, LDD enhanced moth invasion. Model validation showed that including human influence produced more precise and realistic simulations. We provide a powerful and widely applicable methodological framework that stresses the crucial importance of integrating the social landscape to develop accurate invasion models of pest dynamics in complex, agricultural systems.

SimAdapt: an individual-based genetic model for simulating landscape management impacts on populations

Summary 1. Simulation models are essential tools in landscape genetics to study how genetic processes are affected by landscape heterogeneity. However, there is still a need to develop different simulation approaches in landscape genetics, so that users may dispose of additional programs to explore further the impact of land-use and land-cover changes on population genetics. 2. We developed a spatially explicit, individual-based, forward-time, landscape-genetic simulation model combined with a landscape cellular automaton to represent evolutionary processes of adaptation and population dynamics in changing landscapes, using the NetLogo environment. 3. This simulation model represents a unique tool for scientists and scholars looking for a practical and pedagogical framework to explore both empirical and theoretical situations.