The worldwide invasion history of a pest ambrosia beetle inferred using population genomics.

Xylosandrus crassiusculus, a fungus-farming wood borer native to Southeastern Asia, is the most rapidly spreading invasive ambrosia species worldwide. Previous studies focusing on its genetic structure suggested the existence of cryptic genetic variation in this species. Yet, these studies used different genetic markers, focused on different geographical areas and did not include Europe. Our first goal was to determine the worldwide genetic structure of this species based on both mitochondrial and genomic markers. Our second goal was to study X. crassiusculus' invasion history on a global level and identify the origins of the invasion in Europe. We used a COI and RAD sequencing design to characterize 188 and 206 specimens worldwide, building the most comprehensive genetic data set for any ambrosia beetle to date. The results were largely consistent between markers. Two differentiated genetic clusters were invasive, albeit in different regions of the world. The markers were inconsistent only for a few specimens found exclusively in Japan. Mainland USA could have acted as a source for further expansion to Canada and Argentina through stepping stone expansion and bridgehead events. We showed that Europe was only colonized by Cluster II through a complex invasion history including several arrivals from multiple origins in the native area, and possibly including bridgehead from the United States. Our results also suggested that Spain was colonized directly from Italy through intracontinental dispersion. It is unclear whether the mutually exclusive allopatric distribution of the two clusters is due to neutral effects or due to different ecological requirements.

A multi-genome analysis approach enables tracking of the invasion of a single Russian wheat aphid (Diuraphis noxia) clone throughout the New World.

This study investigated the population genetics, demographic history and pathway of invasion of the Russian wheat aphid (RWA) from its native range in Central Asia, the Middle East and Europe to South Africa and the Americas. We screened microsatellite markers, mitochondrial DNA and endosymbiont genes in 504 RWA clones from nineteen populations worldwide. Following pathway analyses of microsatellite and endosymbiont data, we postulate that Turkey and Syria were the most likely sources of invasion to Kenya and South Africa, respectively. Furthermore, we found that one clone transferred between South Africa and the Americas was most likely responsible for the New World invasion. Finally, endosymbiont DNA was found to be a high-resolution population genetic marker, extremely useful for studies of invasion over a relatively short evolutionary history time frame. This study has provided valuable insights into the factors that may have facilitated the recent global invasion by this damaging pest.

Population Genetics of the Blueberry Gall Midge, Dasineura oxycoccana (Diptera: Cecidomyiidae), on Blueberry and Cranberry and Testing Invasion Scenarios.

We compared the population genetic structure between populations of the blueberry gall midge-Dasineura oxycoccana (Johnson) (Diptera: Cecidomyiidae)-from blueberry and cranberry and determined the genetic relationships among geographical subgroups by genotyping 632 individuals from 31 different populations from their native USA regions (New Jersey, Michigan, and Georgia) and from invaded Korean regions using 12 microsatellite loci. Our population genetic analyses showed a clear separation between the two host-associated D. oxycoccana populations from blueberry and cranberry. Using data from only the blueberry-associated D. oxycoccana populations, we identified five genetically isolated subgroups. An analysis of the approximate Bayesian computation suggests that the invasive D. oxycoccana population from Korea appears to have been introduced from an unsampled source population rather than directly from its native range. Our findings will allow for an easier identification of the source of D. oxycoccana into newly invaded regions, as well as to determine their association with blueberry and cranberry, which based on our results can be considered as two distinct species.

Population Genetics for Inferring Introduction Sources of the Oriental Fruit Fly, Bactrocera dorsalis: A Test for Quarantine Use in Korea.

To infer the introduction sources of the oriental fruit fly, Bactrocera dorsalis, we used a mitochondrial marker to reconstruct the haplotype network and 15 microsatellite loci to reveal genetic structure and relationships between the geographically or temporally different collections from Asia. We performed Approximate Bayesian computations to infer a global origin and a source of the quarantine collections found in Korea. As a result, the 40 populations were divided into three groups, of which genetic similarity is not related to the geographic vicinity. Korean samples had a similar genetic structure to Taiwan and Thailand ones. Our results suggest that the place of origin of the B. dorsalis specimens found in Korea's border quarantine is likely to be Taiwan or Thailand. As the global origin of B. dorsalis, we estimated that Taiwan and Thailand were most likely the global origins of Southeast Asian populations by testing hypothetical scenarios by the approximate Bayesian computation analyses. Our results will allow easier identification of the source region of the forthcoming invasion of quarantined B. dorsalis specimens.

Tracing the Origin of Korean Invasive Populations of the Spotted Lanternfly, Lycorma delicatula (Hemiptera: Fulgoridae).

Lycorma delicatula (White) suddenly arrived in Korea where it rapidly spread out in the central region of Korea and caused serious damage to grape vineyards. To trace the source region of its invasiveness, population genetic structures were compared between the native region, China, and the introduced regions, Korea and Japan. We examined 762 individuals from 38 different population collections using 15 microsatellite loci. Both principal coordinate and structure analyses displayed that the Chinese populations were separated into three subgroups which were located significantly far apart from each other. Among them, the Shanghai population was located closest to most Korean populations. Based on the genetic relationships and structures, it was revealed that the multiple introductions into Korea occurred at least three times. In addition, the Shanghai population was strongly estimated to be a source of initial invasive populations of Korea. In addition, analysis of the approximate Bayesian computation suggested simultaneous spread from two distant locations early in the invasion by artificial transportation of the host plants bearing egg masses. Our population genetics study can provide a precedent case with regards to identifying spreads by anthropogenic outcomes in other invasive regions.

Diaphorina citri (Hemiptera: Psylloidea) in China: Two Invasion Routes and Three Transmission Paths.

Diaphorina citri Kuwayama (Hemiptera: Liviidae) is one of the most common pests impacting citrus orchards in southern China. Samples of D. citri were collected in southern China in order to systematically explore the genetic architecture of the species. Mitochondrial cytochrome b (Cytb) and cytochrome coxidase subunit I (COI) were amplified by polymerase chain reaction (PCR) which allowed highlighting low haplotype and nucleotide diversities among the population. Two clades could be observed in the haplotype network. Moreover, Bayesian and maximum parsimony phylogenetic trees were constructed based on the sequences of Cytb and COI. Here, we report on the significant genetic variation of the species when comparing southwestern China with other regions of southern China (southern and southeastern). This analysis also suggested that the genetic structure of D. citri in China originates may from long-term climate fluctuations concomitant with recent disturbances resulting from human activity. Combined with previous data, the present work indicates that D. citri potentially entered China through two distinct invasion routes and spread within the country via three transmission paths.

Invasion origin, rapid population expansion, and the lack of genetic structure of cotton bollworm (Helicoverpa armigera) in the Americas.

In 2013, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) was officially declared as present in Brazil and, after two years, the species was detected in the Caribbean and North America. Information on genetic features and accurate distribution of pests is the basis for agricultural protection policies. Furthermore, such knowledge is imperative to develop control strategies, understand the geographical range, and genetic patterns of this species in the Americas. Here, we carried out the widest sampling of H. armigera in the South American continent and Puerto Rico, after we estimated the diversity, demographic parameters, and genetic structure. The Internal Transcribed Spacer 1 (ITS1) nuclear marker was used to investigate the presence of putative hybrids between H. armigera and H. zea, and they were observed at a frequency of 1.5%. An ABC analysis, based in COI gene fragment, suggested Europe as the origin of South America specimens of H. armigeraand following a movement northward through the Caribbean. Three mtDNA genes and three nDNA markers revealed high genetic diversity distributed without the defined population structure of H. armigera in South America. Most of the genetic variation is within populations with a multidirectional expansion of H. armigera among morphoclimatic regions. High genetic diversity, rapid population expansion, and hybridization have implications for pest management since they suggest that adaptive alleles are spread through wide areas in South America that favor rapid local adaptation of H. armigera to new and disturbed environments (e.g., in agricultural areas).

Simulations indicate that scores of lionfish (Pterois volitans) colonized the Atlantic Ocean.

The invasion of the western Atlantic Ocean by the Indo-Pacific red lionfish (Pterois volitans) has had devastating consequences for marine ecosystems. Estimating the number of colonizing lionfish can be useful in identifying the introduction pathway and can inform policy decisions aimed at preventing similar invasions. It is well-established that at least ten lionfish were initially introduced. However, that estimate has not faced probabilistic scrutiny and is based solely on the number of haplotypes in the maternally-inherited mitochondrial control region. To rigorously estimate the number of lionfish that were introduced, we used a forward-time, Wright-Fisher, population genetic model in concert with a demographic, life-history model to simulate the invasion across a range of source population sizes and colonizing population fecundities. Assuming a balanced sex ratio and no Allee effects, the simulations indicate that the Atlantic population was founded by 118 (54-514, 95% HPD) lionfish from the Indo-Pacific, the Caribbean by 84 (22-328, 95% HPD) lionfish from the Atlantic, and the Gulf of Mexico by at least 114 (no upper bound on 95% HPD) lionfish from the Caribbean. Increasing the size, and therefore diversity, of the Indo-Pacific source population and fecundity of the founding population caused the number of colonists to decrease, but with rapidly diminishing returns. When the simulation was parameterized to minimize the number of colonists (high θ and relative fecundity), 96 (48-216, 95% HPD) colonists were most likely. In a more realistic scenario with Allee effects (e.g., 50% reduction in fecundity) plaguing the colonists, the most likely number of lionfish increased to 272 (106-950, 95% HPD). These results, in combination with other published data, support the hypothesis that lionfish were introduced to the Atlantic via the aquarium trade, rather than shipping. When building the model employed here, we made assumptions that minimize the number of colonists, such as the lionfish being introduced in a single event. While we conservatively modelled the introduction pathway as a single release of lionfish in one location, it is more likely that a combination of smaller and larger releases from a variety of aquarium trade stakeholders occurred near Miami, Florida, which could have led to even larger numbers of colonists than simulated here. Efforts to prevent future invasions via the aquarium trade should focus on the education of stakeholders and the prohibition of release, with adequate rewards for compliance and penalties for violations.

The origin of invasion of an alien frog species in Tibet, China.

Identifying the origins of alien species has important implications for effectively controlling the spread of alien species. The black-spotted frog Pelophylax nigromaculatus, originally from East Asia, has become an alien species on the Tibetan Plateau (TP). In this study, we collected 300 individuals of P. nigromaculatus from 13 native regions and 2 invasive regions (including Nyingchi and Lhasa) on the TP. To identify the source region of the TP introductions, we sequenced portions of the mitochondrial cyt b gene. We sequenced a ∼600-bp portion of the mitochondrial cyt b gene to identify 69 haplotypes (124 polymorphic sites) in all sampled populations. According to the network results, we suggest that the P. nigromaculatus found on the TP was most likely originated from Chongqing by human introduction. Furthermore, we found that the genetic diversity was significantly lower for invasive than for native sites due to founder effects. Our study provides genetic evidence that this alien species invaded the cold environment of high elevations and expanded the distribution of P. nigromaculatus in China.