Genomic signals of local adaptation across climatically heterogenous habitats in an invasive tropical fruit fly (Bactrocera tryoni).

Local adaptation plays a key role in the successful establishment of pest populations in new environments by enabling them to tolerate novel biotic and abiotic conditions experienced outside their native range. However, the genomic underpinnings of such adaptive responses remain unclear, especially for agriculturally important pests. We investigated population genomic signatures in the tropical/subtropical Queensland fruit fly, Bactrocera tryoni, which has an expanded range encompassing temperate and arid zones in Australia, and tropical zones in the Pacific Islands. Using reduced representation sequencing data from 28 populations, we detected allele frequency shifts associated with the native/invasive status of populations and identified environmental factors that have likely driven population differentiation. We also determined that precipitation, temperature, and geographic variables explain allelic shifts across the distribution range of B. tryoni. We found spatial heterogeneity in signatures of local adaptation across various climatic conditions in invaded areas. Specifically, disjunct invasive populations in the tropical Pacific Islands and arid zones of Australia were characterised by multiple significantly differentiated single nucleotide polymorphisms (SNPs), some of which were associated with genes with well-understood function in environmental stress (e.g., heat and desiccation) response. However, invasive populations in southeast Australian temperate zones showed higher gene flow with the native range and lacked a strong local adaptive signal. These results suggest that population connectivity with the native range has differentially affected local adaptive patterns in different invasive populations. Overall, our findings provide insights into the evolutionary underpinnings of invasion success of an important horticultural pest in climatically distinct environments.

Genomic Tools in Biological Invasions: Current State and Future Frontiers.

Human activities are accelerating rates of biological invasions and climate-driven range expansions globally, yet we understand little of how genomic processes facilitate the invasion process. Although most of the literature has focused on underlying phenotypic correlates of invasiveness, advances in genomic technologies are showing a strong link between genomic variation and invasion success. Here, we consider the ability of genomic tools and technologies to (i) inform mechanistic understanding of biological invasions and (ii) solve real-world issues in predicting and managing biological invasions. For both, we examine the current state of the field and discuss how genomics can be leveraged in the future. In addition, we make recommendations pertinent to broader research issues, such as data sovereignty, metadata standards, collaboration, and science communication best practices that will require concerted efforts from the global invasion genomics community.

Current stewardship practices in invasion biology limit the value and secondary use of genomic data.

Invasive species threaten native biota, putting fragile ecosystems at risk and having a large-scale impact on primary industries. Growing trade networks and the popularity of personal travel make incursions a more frequent risk, one only compounded by global climate change. With increasing publication of whole-genome sequences lies an opportunity for cross-species assessment of invasive potential. However, the degree to which published sequences are accompanied by satisfactory spatiotemporal data is unclear. We assessed the metadata associated with 199 whole-genome assemblies of 89 invasive terrestrial invertebrate species and found that only 38% of these were derived from field-collected samples. Seventy-six assemblies (38%) reported an 'undescribed' sample origin and, while further examination of associated literature closed this gap to 23.6%, an absence of spatial data remained for 47 of the total assemblies. Of the 76 assemblies that were ultimately determined to be field-collected, associated metadata relevant for invasion studies was predominantly lacking: only 35% (27 assemblies) provided granular location data, and 33% (n = 25) lacked sufficient collection date information. Our results support recent calls for standardized metadata in genome sequencing data submissions, highlighting the impact of missing metadata on current research in invasion biology (and likely other fields). Notably, large-scale consortia tended to provide the most complete metadata submissions in our analysis-such cross-institutional collaborations can foster a culture of increased adherence to improved metadata submission standards and a standard of metadata stewardship that enables reuse of genomes in invasion science.

Genome-wide analysis reveals distinct global populations of pink bollworm (Pectinophora gossypiella).

The pink bollworm (Pectinophora gossypiella) is one of the world's most destructive pests of cotton. This invasive lepidopteran occurs in nearly all cotton-growing countries. Its presence in the Ord Valley of North West Australia poses a potential threat to the expanding cotton industry there. To assess this threat and better understand population structure of pink bollworm, we analysed genomic data from individuals collected in the field from North West Australia, India, and Pakistan, as well as from four laboratory colonies that originated in the United States. We identified single nucleotide polymorphisms (SNPs) using a reduced-representation, genotyping-by-sequencing technique (DArTseq). The final filtered dataset included 6355 SNPs and 88 individual genomes that clustered into five groups: Australia, India-Pakistan, and three groups from the United States. We also analysed sequences from Genbank for mitochondrial DNA (mtDNA) locus cytochrome c oxidase I (COI) for pink bollworm from six countries. We found low genetic diversity within populations and high differentiation between populations from different continents. The high genetic differentiation between Australia and the other populations and colonies sampled in this study reduces concerns about gene flow to North West Australia, particularly from populations in India and Pakistan that have evolved resistance to transgenic insecticidal cotton. We attribute the observed population structure to pink bollworm's narrow host plant range and limited dispersal between continents.

Population genomic insights into invasion success in a polyphagous agricultural pest, Halyomorpha halys.

Invasive species are increasingly threatening ecosystems and agriculture by rapidly expanding their range and adapting to environmental and human-imposed selective pressures. The genomic mechanisms that underlie such rapid changes remain unclear, especially for agriculturally important pests. Here, we used genome-wide polymorphisms derived from native, invasive, and intercepted samples and populations of the brown marmorated stink bug (BMSB), Halyomorpha halys, to gain insights into population genomics processes that have promoted the successful global invasion of this polyphagous pest. Our analysis demonstrated that BMSB exhibits spatial structure but admixture rates are high among introduced populations, resulting in similar levels of genomic diversity across native and introduced populations. These spatial genomic patterns suggest a complex invasion scenario, potentially with multiple bridgehead events, posing a challenge for accurately assigning BMSB incursions to their source using reduced-representation genomic data. By associating allele frequencies with the invasion status of BMSB populations, we found significantly differentiated single nucleotide polymorphisms (SNPs) located in close proximity to genes for insecticide resistance and olfaction. Comparing variations in allele frequencies among populations for outlier SNPs suggests that BMSB invasion success has probably evolved from standing genetic variation. In addition to being a major nuisance of households, BMSB has caused significant economic losses to agriculture in recent years and continues to expand its range. Despite no record of BMSB insecticide resistance to date, our results show high capacity for potential evolution of such traits, highlighting the need for future sustainable and targeted management strategies.

Southern Hemisphere coasts are biologically connected by frequent, long-distance rafting events.

Globally, species distributions are shifting in response to environmental change,1 and those that cannot disperse risk extinction.2 Many taxa, including marine species, are showing poleward range shifts as the climate warms.3 In the Southern Hemisphere, however, circumpolar oceanic fronts can present barriers to dispersal.4 Although passive, southward movement of species across this barrier has been considered unlikely,5,6 the recent discovery of buoyant kelp rafts on beaches in Antarctica7,8 demonstrates that such journeys are possible. Rafting is a key process by which diverse taxa-including terrestrial, e.g., Lindo,9 Godinot,10 and Censky et al.,11 and marine, e.g., Carlton et al.12 and Gillespie et al.13 species-can cross oceans.14 Kelp rafts can carry passengers7,15-17 and thus can act as vectors for long-distance dispersal of coastal organisms. The small numbers of kelp rafts previously found in Antarctica7,8 do not, however, shed much light on the frequency of such dispersal events.18 We use a combination of high-resolution phylogenomic analyses (>220,000 SNPs) and oceanographic modeling to show that long-distance biological dispersal events in Southern Ocean are not rare. We document tens of kelp (Durvillaea antarctica) rafting events of thousands of kilometers each, over several decades (1950-2019), with many kelp rafts apparently still reproductively viable. Modeling of dispersal trajectories from genomically inferred source locations shows that distant landmasses are well connected, for example South Georgia and New Zealand, and the Kerguelen Islands and Tasmania. Our findings illustrate the power of genomic approaches to track, and modeling to show frequencies of, long-distance dispersal events.

Parallel recolonizations generate distinct genomic sectors in kelp following high-magnitude earthquake disturbance.

Large-scale disturbance events have the potential to drastically reshape biodiversity patterns. Notably, newly vacant habitat space cleared by disturbance can be colonized by multiple lineages, which can lead to the evolution of distinct spatial "sectors" of genetic diversity within a species. We test for disturbance-driven sectoring of genetic diversity in intertidal southern bull kelp, Durvillaea antarctica (Chamisso) Hariot, following the high-magnitude 1855 Wairarapa earthquake in New Zealand. Specifically, we use genotyping-by-sequencing (GBS) to analyse fine-scale population structure across the uplift zone and apply machine learning to assess the fit of alternative recolonizaton models. Our analysis reveals that specimens from the uplift zone carry distinctive genomic signatures potentially linked to post-earthquake recolonization processes. Specifically, our analysis identifies two parapatric spatial-genomic sectors of D. antarctica at Turakirae Head, which experienced the most dramatic uplift. Based on phylogeographical modelling, we infer that bull kelp in the Wellington region was probably a source for recolonization of the heavily uplifted Turakirae Head coastline, via two parallel, eastward recolonization events. By identifying multiple parapatric genotypic sectors within a recently recolonized coastal region, the current study provides support for the hypothesis that competing lineage expansions can generate striking spatial structuring of genetic diversity, even in highly dispersive taxa.

Concordant phylogeographic responses to large-scale coastal disturbance in intertidal macroalgae and their epibiota.

Major ecological disturbance events can provide opportunities to assess multispecies responses to upheaval. In particular, catastrophic disturbances that regionally extirpate habitat-forming species can potentially influence the genetic diversity of large numbers of codistributed taxa. However, due to the rarity of such disturbance events over ecological timeframes, the genetic dynamics of multispecies recolonization processes have remained little understood. Here, we use single nucleotide polymorphism (SNP) data from multiple coastal species to track the dynamics of cocolonization events in response to ancient earthquake disturbance in southern New Zealand. Specifically, we use a comparative phylogeographic approach to understand the extent to which epifauna (with varying ecological associations with their macroalgal hosts) share comparable spatial and temporal recolonization patterns. Our study reveals concordant disturbance-related phylogeographic breaks in two intertidal macroalgal species along with two associated epibiotic species (a chiton and an isopod). By contrast, two codistributed species, one of which is an epibiotic amphipod and the other a subtidal macroalga, show few, if any, genetic effects of palaeoseismic coastal uplift. Phylogeographic model selection reveals similar post-uplift recolonization routes for the epibiotic chiton and isopod and their macroalgal hosts. Additionally, codemographic analyses support synchronous population expansions of these four phylogeographically similar taxa. Our findings indicate that coastal paleoseismic activity has driven concordant impacts on multiple codistributed species, with concerted recolonization events probably facilitated by macroalgal rafting. These results highlight that high-resolution comparative genomic data can help reconstruct concerted multispecies responses to recent ecological disturbance.

The genomic footprint of coastal earthquake uplift.

Theory suggests that catastrophic earth-history events can drive rapid biological evolution, but empirical evidence for such processes is scarce. Destructive geological events such as earthquakes can represent large-scale natural experiments for inferring such evolutionary processes. We capitalized on a major prehistoric (800 yr BP) geological uplift event affecting a southern New Zealand coastline to test for the lasting genomic impacts of disturbance. Genome-wide analyses of three co-distributed keystone kelp taxa revealed that post-earthquake recolonization drove the evolution of novel, large-scale intertidal spatial genetic 'sectors' which are tightly linked to geological fault boundaries. Demographic simulations confirmed that, following widespread extirpation, parallel expansions into newly vacant habitats rapidly restructured genome-wide diversity. Interspecific differences in recolonization mode and tempo reflect differing ecological constraints relating to habitat choice and dispersal capacity among taxa. This study highlights the rapid and enduring evolutionary effects of catastrophic ecosystem disturbance and reveals the key role of range expansion in reshaping spatial genetic patterns.