Loss of genetic diversity and increased embryonic mortality in non-native lizard populations

Many populations are small and isolated with limited genetic variation and high risk of mating with close relatives. Inbreeding depression is suspected to contribute to extinction of wild populations, but the historical and demographic factors that contribute to reduced population viability are often difficult to tease apart. Replicated introduction events in non-native species can offer insights into this problem because they allow us to study how genetic variation and inbreeding depression are affected by demographic events (e.g. bottlenecks), genetic admixture and the extent and duration of isolation. Using detailed knowledge about the introduction history of 21 nonnative populations of the wall lizard Podarcis muralis in England, we show greater loss of genetic diversity (estimated from microsatellite loci) in older populations and in populations from native regions of high diversity. Loss of genetic diversity was accompanied by higher embryonic mortality in non-native populations, suggesting that introduced populations are sufficiently inbred to jeopardize long-term viability. However, there was no statistical correlation between population-level genetic diversity and average embryonic mortality. Similarly, at the individual level, there was no correlation between female heterozygosity and clutch size, infertility or hatching success, or between embryo heterozygosity and mortality. We discuss these results in the context of human-mediated introductions and how the history of introductions can play a fundamental role in influencing individual and population fitness in non-native species

Adaptive responses to cool climate promotes persistence of a non-native lizard

Successful establishment and range expansion of non-native species often require rapid accommodation of novel environments. Here, we use common-garden experiments to demonstrate parallel adaptive evolutionary response to a cool climate in populations of wall lizards (Podarcis muralis) introduced from southern Europe into England. Low soil temperatures in the introduced range delay hatching, which generates directional selection for a shorter incubation period. Non-native lizards from two separate lineages have responded to this selection by retaining their embryos for longer before oviposition-hence reducing the time needed to complete embryogenesis in the nest-and by an increased developmental rate at low temperatures. This divergence mirrors local adaptation across latitudes and altitudes within widely distributed species and suggests that evolutionary responses to climate can be very rapid. When extrapolated to soil temperatures encountered in nests within the introduced range, embryo retention and faster developmental rate result in one to several weeks earlier emergence compared with the ancestral state. We show that this difference translates into substantial survival benefits for offspring. This should promote short- and long-term persistence of non-native populations, and ultimately enable expansion into areas that would be unattainable with incubation duration representative of the native range

Sex, males, and hermaphrodites in the scale insect Icerya purchasi

Funding: This work was supported by a number of fellowships, namely a University Research Fellowship from Royal Society of London (to AG) and a Junior Research Fellowship from Balliol College, Oxford to AG. Funding came from Independent Research Fellowships from Natural Environment Research Council (grant no. NE/K009524/1 to AG and NE/K009516/1 to LR), a Consolidator Grant from European Research Council (grant no. 771387 to AG), a European Research Countil Starting Grant (PGErepro to LR), and a Royal Society Newton fellowship (to LR).Androdioecy (the coexistence of males and hermaphrodites) is a rare mating system for which the evolutionary dynamics are poorly understood. Here we study the only presumed case of androdioecy in insects, found in the cottony cushion scale, Icerya purchasi . In this species, female-like hermaphrodites have been shown to produce sperm and self-fertilize. However, rare males are sometimes observed too. In a large population-genetic analysis, we show for the first time that although self-fertilization appears to be the primary mode of reproduction, rare outbreeding events between males and hermaphrodites do occur, and we thereby confirm androdioecy as the mating system of I. purchasi . Thus, this insect appears to have the colonization advantages of a selfing organism while also benefitting from periodic reintroduction of genetic variation through outbreeding with males.Publisher PDFPeer reviewe

Dispersal Ability Predicts Spatial Genetic Structure in Native Mammals Persisting across an Urbanization Gradient

As the rate of urbanization continues to increase globally, a growing body of research is emerging that investigates how urbanization shapes the movement—and consequent gene flow—of species in cities. Of particular interest are native species that persist in cities, either as small relict populations or as larger populations of synanthropic species that thrive alongside humans in new urban environments. In this study, we used genomic sequence data (SNPs) and spatially explicit individual‐based analyses to directly compare the genetic structure and patterns of gene flow in two small mammals with different dispersal abilities that occupy the same urbanized landscape to evaluate how mobility impacts genetic connectivity. We collected 215 white‐footed mice (Peromyscus leucopus) and 380 big brown bats (Eptesicus fuscus) across an urban‐to‐rural gradient within the Providence, Rhode Island (U.S.A.) metropolitan area (population =1,600,000 people). We found that mice and bats exhibit clear differences in their spatial genetic structure that are consistent with their dispersal abilities, with urbanization having a stronger effect on Peromyscus mice. There were sharp breaks in the genetic structure of mice within the Providence urban core, as well as reduced rates of migration and an increase in inbreeding with more urbanization. In contrast, bats showed very weak genetic structuring across the entire study area, suggesting a near‐panmictic gene pool likely due to the ability to disperse by flight. Genetic diversity remained stable for both species across the study region. Mice also exhibited a stronger reduction in gene flow between island and mainland populations than bats. This study represents one of the first to directly compare multiple species within the same urban‐to‐rural landscape gradient, an important gap to fill for urban ecology and evolution. Moreover, here we document the impacts of dispersal capacity on connectivity for native species that have persisted as the urban landscape matrix expands

Genetics of colonisation in the common wall lizard

In this thesis I set out to further our understanding of the causes and consequences of genetic variation after colonisation events. Specifically, I focused on how historical processes shape genetic diversity and to what extent we can link colonisation history, genetic diversity, individual fitness and population viability. To achieve this, I used a combination of molecular markers, analytical tools and the common wall lizard, Podarcis muralis as a study system. I first infer the origin and genetic architecture of isolated population on islands at the range margin, in relation to mainland populations, to determine whether their current distribution and genetic structure are a result of a historical colonisation event or a more recent introduction. I then unravel the details of human-mediated introductions of P. muralis in England to further test which factors affect their genetic structure. I ask about the contribution of multiple introductions and admixture, the importance of number of founders and the year since their introduction and whether bottleneck events during primary and /or secondary introduction predict the level of genetic diversity in the non-native range. Throughout this study I obtain information on population genetic structure and composition from both native and non-native ranges. This is essential since the (complex) phylogeographic structure of P. muralis in the native range determines the distribution and structure of genetic diversity from which colonists are drawn and the details of colonisation will then reflect in the genetics of non-native populations. Lastly, I assess the consequences of colonisation on reproductive fitness and test for heterozygosity fitness correlations at the individual and population level. Overall, this thesis demonstrates why reconstructing the colonisation history is important when aiming to understand the causes and consequences of genetic variation during colonisation. This information is critical when assessing the relationship between genetic diversity and establishment success. Whether non-native populations have retained sufficient evolutionary potential to adapt to their new climate their long-term viability will be dictated by availability of suitable habitat rather than by internal population factors.</p

Translocation retains genetic diversity of a threatened endemic reptile in Mauritius

The island of Mauritius has experienced five reptile extinctions since the 1600s. Approximately half of the remaining herpetofauna has been restricted to offshore islets, resulting in small populations at high risk of extinction. Under the combined pressures of invasive species, habitat loss and fragmentation and climate change, translocations are considered a powerful tool in conservation of threatened and endangered species. The Bojer's skink, Gongylomorphus bojerii, on the offshore island on Ilot Vacoas represents the remnant population of the species in the southeast of Mauritius. Given the geographic isolation and its genetic distinctiveness, individuals were translocated to the neighbouring island of Ile aux Fouquets in order to re-establish historical range, minimize extinction risk and maintain genetic variation within the species. Using fifteen microsatellite loci, we assessed the genetic structure of the population on Ilot Vacoas in relation to a northern offshore population (on Round Island) and evaluated the genetic consequences of the translocation. Results revealed that the population on Ilot Vacoas exhibits significantly lower levels of genetic variation and strong differentiation (F (ST) = 0.16) compared to the northern population. The inbreeding coefficient was low and no recent bottleneck event was detected from its genetic signature. The translocation on Ile aux Fouquets did not provide evidence of negative genetic effects. The newly established population retained much of the source's genetic material, though the effective population size was found to be relatively small. These findings confirmed the importance of incorporating genetic management and continuous monitoring to detect changes in the long-term survival of translocated populations

Data from: Widespread primary, but geographically restricted secondary, human introductions of wall lizards, Podarcis muralis

Establishing the introduction pathways of alien species is a fundamental task in invasion biology. The common wall lizard, Podarcis muralis, has been widely introduced outside of its native range in both Europe and North America, primarily through escaped pets or deliberate release of animals from captive or wild populations. Here, we use Bayesian clustering, approximate Bayesian computation (ABC) methods and network analyses to reconstruct the origin and colonization history of 23 non-native populations of wall lizards in England. Our analyses show that established populations in southern England originate from at least nine separate sources of animals from native populations in France and Italy. Secondary introductions from previously established non-native populations were supported for eleven (47%) populations. In contrast to the primary introductions, secondary introductions were highly restricted geographically and appear to have occurred within a limited time frame rather than being increasingly common. Together, these data suggest that extant wall lizard populations in England are the result of isolated accidental and deliberate releases of imported animals since the 1970s, with only local translocation of animals from established non-native populations. Given that populations introduced as recently as 25 years ago show evidence of having adapted to cool climate, discouraging further translocations may be important to prevent more extensive establishment on the south coast of England