Population genomic structure of a widespread, urban-dwelling mammal: The eastern grey squirrel (Sciurus carolinensis).

Urbanization is a persistent and widespread driver of global environmental change, potentially shaping evolutionary processes due to genetic drift and reduced gene flow in cities induced by habitat fragmentation and small population sizes. We tested this prediction for the eastern grey squirrel (Sciurus carolinensis), a common and conspicuous forest-dwelling rodent, by obtaining 44K SNPs using reduced representation sequencing (ddRAD) for 403 individuals sampled across the species' native range in eastern North America. We observed moderate levels of genetic diversity, low levels of inbreeding, and only a modest signal of isolation-by-distance. Clustering and migration analyses show that estimated levels of migration and genetic connectivity were higher than expected across cities and forested areas, specifically within the eastern portion of the species' range dominated by urbanization, and genetic connectivity was less than expected within the western range where the landscape is fragmented by agriculture. Landscape genetic methods revealed greater gene flow among individual squirrels in forested regions, which likely provide abundant food and shelter for squirrels. Although gene flow appears to be higher in areas with more tree cover, only slight discontinuities in gene flow suggest eastern grey squirrels have maintained connected populations across urban areas in all but the most heavily fragmented agricultural landscapes. Our results suggest urbanization shapes biological evolution in wildlife species depending strongly on the composition and habitability of the landscape matrix surrounding urban areas.

Development of microsatellite markers for population genetics of biting midges and a potential tool for species identification of Culicoides sonorensis Wirth & Jones.

BACKGROUND: Proper vector surveillance relies on the ability to identify species of interest accurately and efficiently, though this can be difficult in groups containing cryptic species. Culicoides Latreille is a genus of small biting flies responsible for the transmission of numerous pathogens to a multitude of vertebrates. Regarding pathogen transmission, the C. variipennis species complex is of particular interest in North America. Of the six species within this group, only C. sonorensis Wirth & Jones is a proven vector of bluetongue virus and epizootic hemorrhagic disease virus. Unfortunately, subtle morphological differences, cryptic species, and mitonuclear discordance make species identification in the C. variipennis complex challenging. Recently, single-nucleotide polymorphism (SNP) analysis enabled discrimination between the species of this group; however, this demanding approach is not practical for vector surveillance. METHODS: The aim of the current study was to develop a reliable and affordable way of distinguishing between the species within the C. variipennis complex, especially C. sonorensis. Twenty-five putative microsatellite markers were identified using the C. sonorensis genome and tested for amplification within five species of the C. variipennis complex. Machine learning was then used to determine which markers best explain the genetic differentiation between species. This led to the development of a subset of four and seven markers, which were also tested for species differentiation. RESULTS: A total of 21 microsatellite markers were successfully amplified in the species tested. Clustering analyses of all of these markers recovered the same species-level identification as the previous SNP data. Additionally, the subset of seven markers was equally capable of accurately distinguishing between the members of the C. variipennis complex as the 21 microsatellite markers. Finally, one microsatellite marker (C508) was found to be species-specific, only amplifying in the vector species C. sonorensis among the samples tested. CONCLUSIONS: These microsatellites provide an affordable way to distinguish between the sibling species of the C. variipennis complex and could lead to a better understanding of the species dynamics within this group. Additionally, after further testing, marker C508 may allow for the identification of C. sonorensis with a single-tube assay, potentially providing a powerful new tool for vector surveillance in North America.

Consistent signatures of urban adaptation in a native, urban invader ant Tapinoma sessile.

Biological invasions are becoming more prevalent due to the rise of global trade and expansion of urban areas. Ants are among the most prolific invaders with many exhibiting a multiqueen colony structure, dependent colony foundation and reduced internest aggression. Although these characteristics are generally associated with the invasions of exotic ants, they may also facilitate the spread of native ants into novel habitats. Native to diverse habitats across North America, the odorous house ant Tapinoma sessile has become abundant in urban environments throughout the United States. Natural colonies typically have a small workforce, inhabit a single nest, and are headed by a single queen, whereas urban colonies tend to be several orders of magnitude larger, inhabit multiple nests (i.e., polydomy) and are headed by multiple queens (i.e., polygyny). Here, we explore and compare the population genetic and breeding structure of T. sessile within and between urban and natural environments in several localities across its distribution range. We found the social structure of a colony to be a plastic trait in both habitats, although extreme polygyny was confined to urban habitats. Additionally, polydomous colonies were only present in urban habitats, suggesting T. sessile can only achieve supercoloniality within urbanized areas. Finally, we identified strong differentiation between urban and natural populations in each locality and continent-wide, indicating cities may restrict gene flow and exert intense selection pressure. Overall, our study highlights urbanization's influence in charting the evolutionary course for species.

Development of a Set of Microsatellite Markers to Investigate Sexually Antagonistic Selection in the Invasive Ant Nylanderia fulva.

Sexually antagonistic selection (SAS) occurs when distinct alleles are differentially selected in each sex. In the invasive tawny crazy ant, Nylanderia fulva, a genomic region is under SAS, while the rest of the genome is randomly selected in males and females. In this study, we designed a suite of 15 microsatellite markers to study the origin and evolution of SAS in N. fulva. These SAS markers were polymorphic, with allelic frequencies that are highly different between males and females. All haploid males carry only a subset of the alleles present in the population, while females are reliably heterozygous, with one allele from the male gene pool and a different allele inherited from their mother. In addition, we identified six polymorphic markers not associated with SAS and six markers yielding consistent, yet monomorphic, amplification in the introduced range of this species. Reaction condition optimizations allowed all retained markers to be co-amplified in four PCR mixes. The SAS markers may be used to test for the strength and the extent of the genomic regions under SAS in both the native and introduced ranges of N. fulva, while the set of non-SAS loci may be used to assess the invasion route of this species. Overall, the application of these microsatellite markers will yield insights into the origin and evolution of SAS within and among species of the genus Nylanderia.

Extensive human-mediated jump dispersal within and across the native and introduced ranges of the invasive termite Reticulitermes flavipes.

As native ranges are often geographically structured, invasive species originating from a single source population only carry a fraction of the genetic diversity present in their native range. The invasion process is thus often associated with a drastic loss of genetic diversity resulting from a founder event. However, the fraction of diversity brought to the invasive range may vary under different invasion histories, increasing with the size of the propagule, the number of reintroduction events, and/or the total genetic diversity represented by the various source populations in a multiple-introduction scenario. In this study, we generated a SNP data set for the invasive termite Reticulitermes flavipes from 23 native populations in the eastern United States and six introduced populations throughout the world. Using population genetic analyses and approximate Bayesian computation random forest, we investigated its worldwide invasion history. We found a complex invasion pathway with multiple events out of the native range and bridgehead introductions from the introduced population in France. Our data suggest that extensive long-distance jump dispersal appears common in both the native and introduced ranges of this species, probably through human transportation. Overall, our results show that similar to multiple introduction events into the invasive range, admixture in the native range prior to invasion can potentially favour invasion success by increasing the genetic diversity that is later transferred to the introduced range.

Bridgehead effect and multiple introductions shape the global invasion history of a termite.

Native to eastern Asia, the Formosan subterranean termite Coptotermes formosanus (Shiraki) is recognized as one of the 100 worst invasive pests in the world, with established populations in Japan, Hawaii and the southeastern United States. Despite its importance, the native source(s) of C. formosanus introductions and their invasive pathway out of Asia remain elusive. Using ~22,000 SNPs, we retraced the invasion history of this species through approximate Bayesian computation and assessed the consequences of the invasion on its genetic patterns and demography. We show a complex invasion history, where an initial introduction to Hawaii resulted from two distinct introduction events from eastern Asia and the Hong Kong region. The admixed Hawaiian population subsequently served as the source, through a bridgehead, for one introduction to the southeastern US. A separate introduction event from southcentral China subsequently occurred in Florida showing admixture with the first introduction. Overall, these findings further reinforce the pivotal role of bridgeheads in shaping species distributions in the Anthropocene and illustrate that the global distribution of C. formosanus has been shaped by multiple introductions out of China, which may have prevented and possibly reversed the loss of genetic diversity within its invasive range.

The underdog invader: Breeding system and colony genetic structure of the dark rover ant (Brachymyrmex patagonicus Mayr).

Ants are among the most successful species at invading new environments. Their success undeniably comes from their various modes of reproduction and colony breeding structures, which influence their dispersal ability, reproductive potential, and foraging strategies. Almost all invasive ant species studied so far form supercolonies, a dense network of interconnected nests comprising numerous queens, without aggression toward non-nestmates. This strategy results in invasive colonies that are able to grow extremely fast and large while avoiding intraspecific competition, allowing them to monopolize environmental resources and outcompete native species. Here, we developed and used 10 microsatellite markers to investigate the population structure and breeding system of the dark rover ant Brachymyrmex patagonicus Mayr in its introduced range. We determined whether this species exhibits a supercolonial structure by assessing whether different nests belonged to the same genetic colony. We inferred its dispersal ability by investigating isolation by distance and estimated the numbers of queens per colonies and mating per queen through parent-offspring inferences. We found that most of the colonies of B. patagonicus were comprised of a single nest, headed by a single queen. Each nest was distinct from one another, without isolation by distance, which suggests strong dispersal ability through nuptial flights. These features are commonly observed in noninvasive and native ant species, but they are surprising for a successful invasive ant, as they strongly differ from other invasive ants. Overall, we discuss how this seemingly unfavorable strategy for an invasive ant might favor the invasive success of the dark rover ant in the United States.

Sexually antagonistic selection promotes genetic divergence between males and females in an ant.

Genetic diversity acts as a reservoir for potential adaptations, yet selection tends to reduce this diversity over generations. However, sexually antagonistic selection (SAS) may promote diversity by selecting different alleles in each sex. SAS arises when an allele is beneficial to one sex but harmful to the other. Usually, the evolution of sex chromosomes allows each sex to independently reach different optima, thereby circumventing the constraint of a shared autosomal genome. Because the X chromosome is found twice as often in females than males, it represents a hot spot for SAS, offering a refuge for recessive male-beneficial but female-costly alleles. Hymenopteran species do not have sex chromosomes; females are diploid and males are haploid, with sex usually determined by heterozygosity at the complementary sex-determining locus. For this reason, their entire genomes display an X-linked pattern, as every chromosome is found twice as often in females than in males, which theoretically predisposes them to SAS in large parts of their genome. Here we report an instance of sexual divergence in the Hymenoptera, a sexually reproducing group that lacks sex chromosomes. In the invasive ant Nylanderia fulva, a postzygotic SAS leads daughters to preferentially carry alleles from their mothers and sons to preferentially carry alleles from their grandfathers for a substantial region (∼3%) of the genome. This mechanism results in nearly all females being heterozygous at these regions and maintains diversity throughout the population, which may mitigate the effects of a genetic bottleneck following introduction to an exotic area and enhance the invasion success of this ant.