Variation in behavioural traits and their molecular basis in the globally invasive Argentine ant

<p>A salient question in invasion biology is to elucidate what traits make some species invasive and not others. Recently, the introduction process has been hypothesised to function as a filter, selecting for traits that promote invasiveness in introduced populations. Behaviour has been increasingly recognised as a significant driver of animal invasions, but few studies focus on how the introduction process may affect behavioural variation across an invader’s range. This thesis aims at investigating the consequences of the introduction process on behavioural variation along an introduction pathway in the globally widespread Argentine ant. In Chapter I, I investigated transcriptome-wide variations associated with morphological caste as well as worker foraging propensity. I found a number of transcripts showed caste and behaviour-specific expression profiles, and that foraging workers exhibit higher expression of genes related to chemosensory receptors and neurological pathways known to be associated with foraging behaviour and aggression. In chapter II, I investigated octopamine-mediated modulation of foraging behaviour and aggression using pharmacological manipulations using synthetic octopamine (OA) and one of its antagonists. I found that OA was associated with colony-level foraging activity, but did not appear to similarly drive changes in individual behaviour. However, my results suggest that OA is associated with individual aggressiveness, and I also found an association between OA and foraging propensity. In chapter III, I tested the hypothesis that the introduction process selected for increased risk-taking behaviour along the Argentine ant introduction pathway. I used behavioural assays combined with OA diet supplementation in four regions along the introduction pathway, and showed that both behavioural variation and plasticity were consistent across the range, not in support of our hypothesis. Finally, in chapter IV I investigated transcriptome-wide expression profiles in workers along the introduction pathway and discovered distinct transcriptomic signatures associated with range. I found that specific immune and neural pathways were differentially regulated in the introduced range compared to the native range. Overall, my results contribute to a better understanding of caste differentiation and neuromodulation of key behaviours in invasive ants. While I did not find behavioural differentiation between native and invasive Argentine ant populations, I show that they are characterised by specific transcriptomic signatures perhaps underlying the ant’s invasion success. This is one of the first global and integrative studies to focus on changes associated with the introduction of invasive species, and may have important implications for the understanding of biological invasions.</p>

Variation in behavioural traits and their molecular basis in the globally invasive Argentine ant

<p>A salient question in invasion biology is to elucidate what traits make some species invasive and not others. Recently, the introduction process has been hypothesised to function as a filter, selecting for traits that promote invasiveness in introduced populations. Behaviour has been increasingly recognised as a significant driver of animal invasions, but few studies focus on how the introduction process may affect behavioural variation across an invader’s range. This thesis aims at investigating the consequences of the introduction process on behavioural variation along an introduction pathway in the globally widespread Argentine ant. In Chapter I, I investigated transcriptome-wide variations associated with morphological caste as well as worker foraging propensity. I found a number of transcripts showed caste and behaviour-specific expression profiles, and that foraging workers exhibit higher expression of genes related to chemosensory receptors and neurological pathways known to be associated with foraging behaviour and aggression. In chapter II, I investigated octopamine-mediated modulation of foraging behaviour and aggression using pharmacological manipulations using synthetic octopamine (OA) and one of its antagonists. I found that OA was associated with colony-level foraging activity, but did not appear to similarly drive changes in individual behaviour. However, my results suggest that OA is associated with individual aggressiveness, and I also found an association between OA and foraging propensity. In chapter III, I tested the hypothesis that the introduction process selected for increased risk-taking behaviour along the Argentine ant introduction pathway. I used behavioural assays combined with OA diet supplementation in four regions along the introduction pathway, and showed that both behavioural variation and plasticity were consistent across the range, not in support of our hypothesis. Finally, in chapter IV I investigated transcriptome-wide expression profiles in workers along the introduction pathway and discovered distinct transcriptomic signatures associated with range. I found that specific immune and neural pathways were differentially regulated in the introduced range compared to the native range. Overall, my results contribute to a better understanding of caste differentiation and neuromodulation of key behaviours in invasive ants. While I did not find behavioural differentiation between native and invasive Argentine ant populations, I show that they are characterised by specific transcriptomic signatures perhaps underlying the ant’s invasion success. This is one of the first global and integrative studies to focus on changes associated with the introduction of invasive species, and may have important implications for the understanding of biological invasions.</p>

Plant naturalization trends reflect socio-economic history and show a high likelihood of inter-island spread in Hawai‘i

The composition of non-native floras is influenced by a region’s socio-economic history, yet rarely are these factors studied alongside plant naturalization rates over time. Such information is especially critical for archipelagos, which often host large numbers of non-native plants and would benefit from preventing inter-island spread. We compiled the first record of occurrence and first record of naturalization for all naturalized plants in Hawai‘i alongside data on their origin, native climate types, taxonomy, and likely introduction pathway, and compared rates of naturalization with socio-economic trends. We found that the rate of total plant naturalizations has increased at a roughly constant rate during the past century without any sign of plateauing. However, this relatively steady increase is underlain by notable fluctuations in naturalization rates for different introduction pathways, with ornamentals increasing recently while agriculture-related plants have decreased. Furthermore, this trend mirrors a shift from an agriculture-dominated economy to a tourism-based one associated with increases in both resident and tourist populations as well as general economic well-being. We further found that the average naturalized species spreads at a rate of 1.86 islands per decade, eventually occupying most major islands in the archipelago, and the rate of spread appears to be increasing since Hawai‘i’s economic shift. Our findings also emphasize the diversity of Hawai‘i’s non-native flora, which originates from a variety of climates, continents, and taxonomic groups. We demonstrated that many non-native species have native ranges that include temperate climates, which is important because these climates typically co-occur with higher elevation, remnant patches of native-dominated ecosystems in Hawai‘i’. This study reveals trends that may help predict a species’ ability to naturalize and spread within and between islands, and we discuss management implications that may be extended to other regions.

Alien plants of Europe: introduction pathways, gateways and time trends

The Convention on Biological Diversity (CBD) pathways classification framework used in the implementation of the European Union’s (EU) Regulation 1143/2014 on invasive alien species (IAS Regulation) has recently been adopted by the European Alien Species Information Network (EASIN), the official information system supporting the implementation of the IAS Regulation. In the current paper, the result of an alignment of the primary introduction pathways of all alien plants in Europe included in the EASIN catalogue is presented, based on the CBD framework. In total, 6,250 alien plant taxa (marine plants excluded), both alien to Europe (native range outside Europe) and alien in Europe (native range partially in Europe) are reported. Altogether 5,175 plant taxa had their primary introduction pathway aligned based on the CBD framework, while for the rest the pathway remains unknown. In addition, the taxonomy, year and country of its first record in the wild are provided for each taxon. Our analyses reveal that the main primary introduction pathways of alien plants into Europe are linked to accidental escapes from ornamental and horticultural activities. Northwestern European countries seem to act as the main gateway areas of alien plants into Europe. Recent first observations of new alien taxa growing spontaneously exhibit a contemporary accelerating trend for plants alien to Europe, particularly linked to ornamental and horticultural activities. On the other hand, the number of new plants alien in Europe seems to have stabilized over the last few decades. The present work can assist in the prioritization of introduction pathways control, with the target of slowing down the rate of alien plants introductions into Europe, following also the requirements of the IAS Regulation.

Introduction bias: Imbalance in species introductions may obscure the identification of traits associated with invasiveness

The introduction stage is usually overlooked in trait-based studies of invasiveness, implicitly assuming that species introductions are random. However, human activities promote the movement of specific types of species. Thus, species deliberately introduced for distinct purposes (e.g. gardening, forestry) or as contaminants of human commodities (e.g. stowaway) will likely show particular traits. If species with certain traits have been preferentially introduced (i.e. introduction bias), some traits may have been mistakenly linked to species' invasion abilities due to their influence on introduction probability. In this work, we propose a theoretical framework with different scenarios of introduction bias. The introduction scenarios are: (1) Random introduction, independent from traits; (2) Biologically biased introduction, following the worldwide distribution of the trait; and (3) Human biased introduction, following a theoretical introduction pathway that favours the introduction of species with high values of the trait. We evaluate how the introduced trait distributions in these scenarios may affect trait distributions in naturalized and invasive species pools under different hypothesized associations between traits and the probabilities of naturalization and invasion. The aim of this work is to identify situations where ignoring introduction bias may lead to spurious correlations being found between species' traits and species' ability to become naturalized or invasive. Our framework strongly points to the need to evaluate the traits of species that have become naturalized or invasive along with the traits of species that have failed to do so in order to unravel any existing introduction bias that may confound the correlation between species' traits and invasion success. Overlooking a possible introduction bias may lead to the overestimation of the correlation between the trait and the species' invasion ability, especially in cases when the pool of introduced species shows extreme values of the trait distribution (as compared to a random introduction). Trait-based studies that deserve special attention to avoid undesired effects of introduction bias on their findings are: those that investigate naturalization using only the pool of naturalized species, and those studies that examine invasiveness by comparing invasive species with native species.

Genome Sequence Resource of ‘Candidatus Liberibacter asiaticus’ from Diaphorina citri Kuwayama (Hemiptera: Liviidae) in Colombia

‘Candidatus Liberibacter asiaticus’ (CLas) is an unculturable phloem-restricted α-proteobacterium associated with huanglongbing (HLB). Here, we provide the genome sequence of CLas strain CoFLP1 from its insect vector Diaphorina citri (Hemiptera: Liviidae) collected in the department of La Guajira, Colombia. The CoFLP1 strain is composed of 1,231,639 bp with G+C 36.5% content. This study reports the first CLas genome sequence from Colombia, which will add to CLas genome resources and help to elucidate our understanding of the introduction pathway of HLB in South America.

Genome Sequence Resource of ‘Candidatus Liberibacter asiaticus’ from Diaphorina citri Kuwayama (Hemiptera: Liviidae) from La Réunion

‘Candidatus Liberibacter asiaticus’ (CLas) is an insect-transmitted, phloem-restricted α-proteobacterium associated with huanglongbing (HLB). Here, we provide the whole genome sequence of CLas strain, ReuSP1, from its insect vector Diaphorina citri (Hemiptera: Liviidae) collected in La Réunion. The genome is composed of 1,230,064 bp and has a 36.5% G+C content. This study reports the first CLas genome sequence from La Réunion, which will add to CLas genome resources and help elucidate our understanding of the introduction pathway into La Réunion.

Classifying the introduction pathways of alien species: are we moving in the right direction?

Alien species are introduced to new regions in many different ways and for different purposes. A number of frameworks have been developed to group such pathways of introduction into discrete categories in order to improve our understanding of biological invasions, provide information for interventions that aim to prevent introductions, enable reporting to national and international organisations and facilitate the prediction of threats. The introduction pathway classification framework proposed by the Convention on Biological Diversity (CBD) as a global standard is comprised of six main categories and 44 sub-categories. However, issues have arisen with its implementation. In this position paper, we outline five desirable properties of an introduction pathway classification framework – it should be compatible (i.e. the level of detail of the categories is similar to that of the available data), actionable (i.e. categories link to specific interventions), general (i.e. categories are applicable across the contexts that are of interest (e.g. taxa, habitats and regions)), equivalent (i.e. categories are equivalent in their level of detail) and distinct (i.e. categories are discrete and easily distinguished) – termed the CAGED properties. The six main categories of the CBD framework have all of the CAGED properties, but the detailed sub-categories have few. Therefore, while the framework has been proposed by the CBD as a global standard and efforts have been made to put it into practice, we argue that there is room for improvement. We conclude by presenting scenarios for how the issues identified could be addressed, noting that a hybrid model might be most appropriate.

Implementing Low-Cost, High Accuracy DNA Barcoding From Single Molecule Sequencing to Screen Larval Tephritid Fruit Flies Intercepted at Ports of Entry

Exotic fruit flies in the family Tephritidae pose a threat to U.S. agriculture and natural resources. As part of ongoing fruit fly detection and exclusion programs, invasive fruit fly adults are periodically trapped in and introduced populations are eradicated from two major fruit producing states: California and Florida. Although the pathways used by flies to enter these states are not clear, one possible introduction pathway is hand-carrying fruits and vegetables infested with eggs or larvae through ports of entry during border crossings or international air travel. These collections represent an important resource for determining what species are most commonly associated with particular ports of entry, their host plants, and source country, making the identification of the intercepted larvae fundamental. Here, we examine cytochrome c oxidase subunit I sequences obtained with Sanger DNA sequencing and Single Molecule Real-time sequencing (SMRT) technologies on a collection of hundreds of intercepted larvae and pupae that are suspected to be fruit pests found in the subfamily Dacinae, in addition to a collection of field-caught flies. Utilizing Pacific Biosciences (PacBio) Circular Consensus Sequencing, we sequenced thousands of independent amplicons in a single SMRT cell. We present our implementation of PacBio’s method by describing wet-lab procedures as well as analytical protocols to automate the process. Finally, for the intercepted material, we compared the generated SMRT data to sequences produced with Sanger and evaluate their quality as a means to identify flies. Using intercepted material, we obtained a sequencing success of over 88% with PacBio’s SMRT sequencing. As the spread of invasive insects grow, so will the size of collections of intercepted material; we found technologies such as SMRT sequencing to be excellent resources to simplify the generation of large amounts of molecular data and to reduce or eliminate all together the manipulation of the sequences.

The significance of anthropochory in Hercinothrips femoralis (Thysanoptera: Thripidae) – Short Communication

After the first record of the banded greenhouse thrips, Hercinothrips femoralis (Reuter, 1891) in Slovakia in 2008, a peculiar occurrence in an extreme subalpine environment of Podbanské (High Tatra Mts.), Slovakia, during the summer of the same year was observed. Since this species of exotic thrips is known to be almost sedentary, the mode of dispersal was hypothesized to be related to passive transport via weather currents. According to our observations of unintentional dispersal a test was conducted to research a previously unidentified introduction pathway of this species. Our preliminary results show that passive transport by humans plays a crucial role in the dispersal of H. femoralis.