Invasion genomics uncover contrasting scenarios of genetic diversity in a widespread marine invader

Invasion rates have increased in the past 100 y irrespective of international conventions. What characterizes a successful invasion event? And how does genetic diversity translate into invasion success? Employing a whole-genome perspective using one of the most successful marine invasive species world-wide as a model, we resolve temporal invasion dynamics during independent invasion events in Eurasia. We reveal complex regionally independent invasion histories including cases of recurrent translocations, time-limited translocations, and stepping-stone range expansions with severe bottlenecks within the same species. Irrespective of these different invasion dynamics, which lead to contrasting patterns of genetic diversity, all nonindigenous populations are similarly successful. This illustrates that genetic diversity, per se, is not necessarily the driving force behind invasion success. Other factors such as propagule pressure and repeated introductions are an important contribution to facilitate successful invasions. This calls into question the dominant paradigm of the genetic paradox of invasions, i.e., the successful establishment of nonindigenous populations with low levels of genetic diversity.

The role of propagule pressure and environmental factors on the establishment of a large invasive cyprinid: black carp in the Laurentian Great Lakes basin

Understanding the factors underlying species establishment is critical for the management of invasive fishes, yet the roles of propagule pressure and environmental factors are infrequently quantified in joint models. We estimated the establishment likelihood of the invasive black carp (Mylopharyngodon piceus) by examining the relative influence of propagule pressure (introduction size and age structure) and environmental factors (temperature-driven young-of-year [YOY] overwinter survival, adult survival, age at maturity, and longevity). Simulations demonstrated that both propagule pressure and environmental factors can act as non-linear bottlenecks to establishment. When the model was applied to 12 Great Lakes tributaries and nearshore areas, black carp establishment was probable with sufficient propagules and under most environmental conditions (median p = 0.21–0.73, 0.70–1.00, and 0.46–0.97 for 100 pairs of age 4, age 9, and age 16 fish, respectively), except for YOY (p < 0.01). Our analysis is one of the few studies to examine the relative role of propagule pressure and environmental conditions on establishment, indicating that both factors can lead to establishment failure independently or concurrently within an ecosystem.

Genetic Factors Associated with Variation in Abundance of the Invasive Yellow Crazy Ant (Anoplolepis gracilipes)

<p>A key component of successful invasion is the ability of an introduced population to reach sufficient abundance to persist, spread, and alter or dominate the recipient biological community. Genetic diversity is one of many factors that may contribute to population dynamics, but has important ramifications for biological fitness, and thus invasion success in the long term. I explored genetic factors associated with variation in abundance (i.e., differential invasion success) of the yellow crazy ant Anoplolepis gracilipes in the Indo-Pacific region, primarily focussing on Arnhem Land in Australia's Northern Territory. I explored five aspects that I hypothesised could contribute to variation in the abundance of this ant: 1) I investigated the unusual reproductive mode of A. gracilipes, and tested whether it involved dependent-lineage genetic caste determination (DL GCD) in Arnhem Land. In DL GCD systems populations require hybridisation between genetically distinct groups to produce both reproductive and worker castes. Asymmetry in the ratio of different lineages may result in low abundance and population collapse. I found no evidence for a DL GCD system in A. gracilipes, and thus its abundance in Arnhem Land does not appear to be constrained by any lineage ratio asymmetry. Worker reproduction (either of males or asexual production of other workers) also appeared unlikely. The reproductive mode of the species remains fascinating but enigmatic; 2) I explored whether multiple source populations were responsible for the observed variation in abundance in Arnhem Land (i.e., is abundance associated with propagule pressure, or populations from different sources), and if the population has diverged since introduction. The A. gracilipes population in Arnhem Land stemmed from a single source, and thus propagule pressure was apparently not responsible for variation in abundance. In contrast to many invasive ants, population divergence has occurred since introduction; 3) I tested the hypotheses that genetic variation was associated with variation in abundance in Arnhem Land, and that ecological success was density-dependent. While the population divergence found in Chapter 3 was not related to variation in abundance, genotypic diversity was higher in more abundant nest clusters. These more abundant nest clusters were in turn associated with lower native ant species diversity, and a difference in composition of the invaded ant community (i.e., greater ecological success); 4) I revisited the invasion of the yellow crazy ant in Tokelau to determine whether a haplotype that was linked to greater abundance and dominance of the ant community has increased in distribution. Although ants of the inferred dominant haplotype were implicated in most new invasions, their abundance was substantially lower than previously observed in Tokelau; 5) I conducted a preliminary analysis of the metagenomic diversity of A. gracilipes endogenous parasites and symbionts among populations from Christmas Island, Okinawa, Samoa and Arnhem Land. Bacterial community composition and diversity differed between the study populations. Variation in abundance among A. gracilipes populations in Arnhem Land was not due to parasite load on populations with low abundance. However, low abundance of A. gracilipes was correlated with lower microbial diversity overall, and higher prevalence of some groups, notably two that confer antibiotic properties. Together, my findings suggest that propagule pressure, reproductive mode and haplotype-specific effects do not appear to be associated with variation in A. gracilipes abundance. Other genetic factors I investigated do appear to be associated with the variation in A. gracilipes abundance and effects on the invaded ant communities. Genotypic diversity was positively related to the abundance of A. gracilipes in Arnhem Land, and this relationship may be affected by population divergence through population bottlenecks. In addition, differences in bacterial diversity among populations highlighted several candidate bacteria that could be associated with variation in abundance, which would be a topic of future work. Although genetic factors are often implicated in the successful establishment of invasive species, my thesis demonstrates that genetic factors may also be associated with post-establishment population dynamics.</p>

Genetic Factors Associated with Variation in Abundance of the Invasive Yellow Crazy Ant (Anoplolepis gracilipes)

<p>A key component of successful invasion is the ability of an introduced population to reach sufficient abundance to persist, spread, and alter or dominate the recipient biological community. Genetic diversity is one of many factors that may contribute to population dynamics, but has important ramifications for biological fitness, and thus invasion success in the long term. I explored genetic factors associated with variation in abundance (i.e., differential invasion success) of the yellow crazy ant Anoplolepis gracilipes in the Indo-Pacific region, primarily focussing on Arnhem Land in Australia's Northern Territory. I explored five aspects that I hypothesised could contribute to variation in the abundance of this ant: 1) I investigated the unusual reproductive mode of A. gracilipes, and tested whether it involved dependent-lineage genetic caste determination (DL GCD) in Arnhem Land. In DL GCD systems populations require hybridisation between genetically distinct groups to produce both reproductive and worker castes. Asymmetry in the ratio of different lineages may result in low abundance and population collapse. I found no evidence for a DL GCD system in A. gracilipes, and thus its abundance in Arnhem Land does not appear to be constrained by any lineage ratio asymmetry. Worker reproduction (either of males or asexual production of other workers) also appeared unlikely. The reproductive mode of the species remains fascinating but enigmatic; 2) I explored whether multiple source populations were responsible for the observed variation in abundance in Arnhem Land (i.e., is abundance associated with propagule pressure, or populations from different sources), and if the population has diverged since introduction. The A. gracilipes population in Arnhem Land stemmed from a single source, and thus propagule pressure was apparently not responsible for variation in abundance. In contrast to many invasive ants, population divergence has occurred since introduction; 3) I tested the hypotheses that genetic variation was associated with variation in abundance in Arnhem Land, and that ecological success was density-dependent. While the population divergence found in Chapter 3 was not related to variation in abundance, genotypic diversity was higher in more abundant nest clusters. These more abundant nest clusters were in turn associated with lower native ant species diversity, and a difference in composition of the invaded ant community (i.e., greater ecological success); 4) I revisited the invasion of the yellow crazy ant in Tokelau to determine whether a haplotype that was linked to greater abundance and dominance of the ant community has increased in distribution. Although ants of the inferred dominant haplotype were implicated in most new invasions, their abundance was substantially lower than previously observed in Tokelau; 5) I conducted a preliminary analysis of the metagenomic diversity of A. gracilipes endogenous parasites and symbionts among populations from Christmas Island, Okinawa, Samoa and Arnhem Land. Bacterial community composition and diversity differed between the study populations. Variation in abundance among A. gracilipes populations in Arnhem Land was not due to parasite load on populations with low abundance. However, low abundance of A. gracilipes was correlated with lower microbial diversity overall, and higher prevalence of some groups, notably two that confer antibiotic properties. Together, my findings suggest that propagule pressure, reproductive mode and haplotype-specific effects do not appear to be associated with variation in A. gracilipes abundance. Other genetic factors I investigated do appear to be associated with the variation in A. gracilipes abundance and effects on the invaded ant communities. Genotypic diversity was positively related to the abundance of A. gracilipes in Arnhem Land, and this relationship may be affected by population divergence through population bottlenecks. In addition, differences in bacterial diversity among populations highlighted several candidate bacteria that could be associated with variation in abundance, which would be a topic of future work. Although genetic factors are often implicated in the successful establishment of invasive species, my thesis demonstrates that genetic factors may also be associated with post-establishment population dynamics.</p>

Exotic Reptiles in the Pet Trade: Are They a Threat to New Zealand?

<p>Worldwide, invasive species are associated with severe ecological and economic impacts. As a group, reptiles are very successful invaders and in some areas where they have established they are responsible for the decline of native fauna and economic disruptions, whilst also posing a threat to human health. Due to its biogeographical isolation and unique evolutionary history, New Zealand is highly susceptible to invasive species. Importation of reptiles into New Zealand is illegal, however over a dozen species of exotic reptile are legally present in captivity and their risk of establishment is unknown. This study investigates their establishment potential and possible impacts by considering 1) the amount of trade and propagule pressure of species, 2) the degree of climate match between their native range and New Zealand, 3) areas that may be suitable for establishment based on physiological models of incubation and development, 4) their ability to transfer pathogens to native fauna and humans, and 5) overall establishment risk. The red-eared slider (Trachemys scripta elegans; RES) is the most common and easily obtained exotic reptile pet in New Zealand, with over 800 sales per annum. The RES is also the species most regularly released into the wild. Climate matching models in this study were developed to minimise false-negative predictions, to generate a suitability score irrespective of the prevalence of species records (allowing species to be easily compared to one another), and incorporated a weighted multimodel average prediction based on the relative importance of climatic variables to each species. These correlative models indicated that the blotched blue-tongue skink (Tiliqua nigrolutea) had the highest degree of climate match with parts of New Zealand, while the common blue-tongue skink (T. scincoides) had the highest proportion of land area predicted to be suitable for establishment. The other 10 species generally had both low climate match scores and limited areas within New Zealand predicted to be suitable. Mechanistic models focus upon environmental influences on physiological processes of a species, such as development and growth. Degree-day models, combined with soil measurements in potential reptile nesting sites in New Zealand, were utilised to determine if environmental conditions were suitable for the successful reproduction of oviparous exotic reptiles. These models predicted that the New Zealand environment meets the minimum thermal requirements for the incubation of eggs of RES, snake-neck turtles (Chelodina longicollis), and Reeves turtles (Chinemys reevesii). While prevalence of Salmonella in exotic reptiles is higher than that of native reptiles, it is considerably lower than that of exotic reptiles overseas. All serovars identified in this study had been previously reported both in humans and reptiles in New Zealand. The overall risk assessment for 12 species of exotic reptile kept in captivity in New Zealand indicates that blotched blue-tongue skinks and RES pose the highest establishment risk. Blotched blue-tongue skinks are allegedly only present in zoos. Therefore, based on propagule pressure, RES pose the highest establishment risk and efforts should focus on minimising release events and removing feral individuals from the New Zealand environment. In summary, at least eight species of exotic reptile legally traded within New Zealand are predicted to be capable of surviving in a portion of the New Zealand environment and at least three species have the potential to successfully breed in warmer microclimates. However, further research involving climatic tolerances and breeding potential (i.e., soil moisture content, juvenile survival, sex ratio, and predicted climate change) is recommended. Public education and possible regulations imposed on the New Zealand exotic reptile trade may prevent introductions of these species into the local environment and still allow selected species to be enjoyed by the New Zealand public. The methods developed in this study may be easily applied to other species and other geographic regions, allowing investigation into the establishment risk of alien species. This may help guide control and management efforts and help stem the tide of the growing problem of invasive species.</p>

Exotic Reptiles in the Pet Trade: Are They a Threat to New Zealand?

<p>Worldwide, invasive species are associated with severe ecological and economic impacts. As a group, reptiles are very successful invaders and in some areas where they have established they are responsible for the decline of native fauna and economic disruptions, whilst also posing a threat to human health. Due to its biogeographical isolation and unique evolutionary history, New Zealand is highly susceptible to invasive species. Importation of reptiles into New Zealand is illegal, however over a dozen species of exotic reptile are legally present in captivity and their risk of establishment is unknown. This study investigates their establishment potential and possible impacts by considering 1) the amount of trade and propagule pressure of species, 2) the degree of climate match between their native range and New Zealand, 3) areas that may be suitable for establishment based on physiological models of incubation and development, 4) their ability to transfer pathogens to native fauna and humans, and 5) overall establishment risk. The red-eared slider (Trachemys scripta elegans; RES) is the most common and easily obtained exotic reptile pet in New Zealand, with over 800 sales per annum. The RES is also the species most regularly released into the wild. Climate matching models in this study were developed to minimise false-negative predictions, to generate a suitability score irrespective of the prevalence of species records (allowing species to be easily compared to one another), and incorporated a weighted multimodel average prediction based on the relative importance of climatic variables to each species. These correlative models indicated that the blotched blue-tongue skink (Tiliqua nigrolutea) had the highest degree of climate match with parts of New Zealand, while the common blue-tongue skink (T. scincoides) had the highest proportion of land area predicted to be suitable for establishment. The other 10 species generally had both low climate match scores and limited areas within New Zealand predicted to be suitable. Mechanistic models focus upon environmental influences on physiological processes of a species, such as development and growth. Degree-day models, combined with soil measurements in potential reptile nesting sites in New Zealand, were utilised to determine if environmental conditions were suitable for the successful reproduction of oviparous exotic reptiles. These models predicted that the New Zealand environment meets the minimum thermal requirements for the incubation of eggs of RES, snake-neck turtles (Chelodina longicollis), and Reeves turtles (Chinemys reevesii). While prevalence of Salmonella in exotic reptiles is higher than that of native reptiles, it is considerably lower than that of exotic reptiles overseas. All serovars identified in this study had been previously reported both in humans and reptiles in New Zealand. The overall risk assessment for 12 species of exotic reptile kept in captivity in New Zealand indicates that blotched blue-tongue skinks and RES pose the highest establishment risk. Blotched blue-tongue skinks are allegedly only present in zoos. Therefore, based on propagule pressure, RES pose the highest establishment risk and efforts should focus on minimising release events and removing feral individuals from the New Zealand environment. In summary, at least eight species of exotic reptile legally traded within New Zealand are predicted to be capable of surviving in a portion of the New Zealand environment and at least three species have the potential to successfully breed in warmer microclimates. However, further research involving climatic tolerances and breeding potential (i.e., soil moisture content, juvenile survival, sex ratio, and predicted climate change) is recommended. Public education and possible regulations imposed on the New Zealand exotic reptile trade may prevent introductions of these species into the local environment and still allow selected species to be enjoyed by the New Zealand public. The methods developed in this study may be easily applied to other species and other geographic regions, allowing investigation into the establishment risk of alien species. This may help guide control and management efforts and help stem the tide of the growing problem of invasive species.</p>

Jack, Master or Both? The Invasive Ladybird Harmonia Axyridis Outperforms Its Native Counterpart Despite Similar Levels of Plasticity

The plasticity of performance traits is expected to promote the successful invasion of species. Therefore, the comparison of reaction norms of invasive species with native competitors should enhance predictions of alien species establishment. Yet, most studies focus on a reduced set of traits, rarely in combination, or do not include trait variability to make predictions of establishment success. Here, we acclimated individuals to a cold, medium or warm temperature regime and measured critical thermal limits, life-history traits, and starvation resistance of the globally invasive Harmonia axyridis and its native counterpart Cheilomenes lunata. The native C. lunata had higher thermal plasticity of starvation resistance and higher upper thermal tolerance than H. axyridis. By contrast, H. axyridis outperformed C. lunata in most life-history traits. We combined trait responses, transport duration and propagule pressure to simulate the final number of beetles established in the introduced site in cold, medium and warm scenarios, where beetles also experienced a heatwave once established. Although C. lunata initially outcompeted the invasive species during transport, more H. axyridis survived in all environments because of higher life-history trait responses, in particular, higher fecundity. Despite increased starvation mortality in the warm scenario, H. axyridis established successfully given sufficient propagule size. By contrast, in the event of a heatwave, H. axyridis numbers plummeted and higher numbers of the native species established in the cold scenario. This study underscores the importance of considering a combination of traits and respective cascading effects when estimating the establishment potential of species and responses to climate warming.

Are Introduced Alien Species More Predisposed to Invasion in Recipient Environments If They Provide a Wider Range of Services to Humans?

The drivers of invasion success of alien species remain, to some extent, a matter of debate. Here, we suggest that the services (the benefits humans obtain from a species) provided by alien plants could predict their invasion status, such that alien species providing more services would be more likely to be invasive than not. The rationale for this expectation is that alien species providing multiple services stand a better chance of being introduced in various numbers and multiple times outside their native range (propagule pressure theory). We investigated this hypothesis on alien woody species in South Africa. First, we defined 12 services provided by all the 210 known naturalized alien woody plants in South Africa. Then, we tested for a phylogenetic signal in these services using a DNA barcode-based phylogeny. Finally, we tested for potential links between the services and invasion status by fitting GLM models with appropriate error families. We found a phylogenetic signal in most services, suggesting that closely related species tend to provide similar services. Counter-intuitively, we consistently found that alien non-invasive species tend to provide more services, or even unique services, in comparison to alien invasive species. Although alternative scenarios are plausible to explain this unexpected finding, we speculate that harvesting alien plants for human benefits may limit their invasion ability. This warrants further investigation.

Patterns and drivers of native, non-native, and at-risk freshwater fish richness in Canada

Understanding the relative roles of the historical, environmental, and anthropogenic processes underlying spatial biodiversity patterns is crucial to predict the impacts of global environmental changes. We quantified the relative roles of these factors in influencing species richness of total, native, non-native, and at-risk freshwater fishes in 985 tertiary watersheds across Canada, while accounting for correlations among descriptors and spatial autocorrelation. Our findings indicate differences in factors influencing richness patterns among species categories. Environmental factors related to energy availability and historical factors related to post-glacial recolonization both played roles in shaping spatial variation in native species richness. In contrast, variation in non-native species richness was largely related to human activities increasing propagule pressure and habitat disturbance, which were greater for foreign species (i.e. not native to Canada) than for translocated native species. Anthropogenic processes and environmental conditions were both important determinants of at-risk species richness. Our study emphasizes the importance of an integrated approach that simultaneously considers natural and anthropogenic processes to better predict the fish biodiversity change at the landscape scale.