Does urbanisation lead to parallel demographic shifts across the world in a cosmopolitan plant?

Urbanisation is occurring globally, leading to dramatic environmental changes that are altering the ecology and evolution of species. In particular, the expansion of human infrastructure and the loss and fragmentation of natural habitats in cities is predicted to increase genetic drift and reduce gene flow by reducing the size and connectivity of populations. Alternatively, the 'urban facilitation model' suggests that some species will have greater gene flow into and within cities leading to higher diversity and lower differentiation in urban populations. These alternative hypotheses have not been contrasted across multiple cities. Here, we used the genomic data from the GLobal Urban Evolution project (GLUE), to study the effects of urbanisation on non-adaptive evolutionary processes of white clover (Trifolium repens) at a global scale. We found that white clover populations presented high genetic diversity and no evidence of reduced Ne linked to urbanisation. On the contrary, we found that urban populations were less likely to experience a recent decrease in effective population size than rural ones. In addition, we found little genetic structure among populations both globally and between urban and rural populations, which showed extensive gene flow between habitats. Interestingly, white clover displayed overall higher gene flow within urban areas than within rural habitats. Our study provides the largest comprehensive test of the demographic effects of urbanisation. Our results contrast with the common perception that heavily altered and fragmented urban environments will reduce the effective population size and genetic diversity of populations and contribute to their isolation.

The role of divergent host use and geography in the evolution of habitat isolation and sexual isolation among sister species of Belonocnema gall wasps.

Ecology and geography can play important roles in the evolution of reproductive isolation across the speciation continuum, but few studies address both at the later stages of speciation. This notable gap in knowledge arises from the fact that traditional ecological speciation studies have predominantly focused on the role of ecology in initiating the speciation process, while many studies exploring the effect of geography (e.g., reinforcement) concentrate on species pairs that lack divergent ecological characteristics. We simultaneously examine the strength of habitat isolation and sexual isolation among three closely related species of Belonocnema gall-forming wasps on two species of live oaks, Quercus virginiana and Q. geminata, that experience divergent selection from their host plants and variable rates of migration due to their geographic context. We find that the strength of both habitat isolation and sexual isolation is lowest among allopatric species pairs with the same host plant association, followed by allopatric species with different host plant associations, and highest between sympatric species with different host-plant associations. This pattern suggests that divergent selection due to different host use interacts with geography in the evolution of habitat isolation and sexual isolation during the later stages of speciation of Belonocnema wasps.

A test of trade-offs in dispersal and reproduction within and between a sister species pair of specialist insect herbivores.

Understanding the drivers of trade-offs among traits is vital for comprehending the evolution and maintenance of trait variation. Theoretical frameworks propose that evolutionary mechanisms governing trade-offs frequently exhibit a scale-dependent nature. However, empirical tests of whether trade-offs exhibited across various biological scales (i.e. individuals, populations, species, genera, etc.) remains scarce. In this study, we explore trade-off between dispersal and reproductive effort among sympatric sister species of wasps in the genus Belonocnema (Hymenoptera: Cynipini: Cynipidae) that form galls on live oaks: B. fossoria, which specializes on Quercus geminata, and B. treatae, which specializes on Q. virginiana. Specifically, our results suggest that B. fossoria has evolved reduced flight capability and smaller wings, but a larger abdomen and greater total reproductive effort than B. treatae, which has larger wings and is a stronger flier, but has a smaller abdomen and reduced total reproductive effort. These traits and the relationships among them remain unchanged when B. fossoria and B. treatae are transplanted and reared onto the alternative host plant, suggesting that trait divergence is genetically based as opposed to being a plastic response to the different rearing environments. However, when looking within species, we found no evidence of intraspecific trade-offs between wing length and reproductive traits within either B. fossoria or B. treatae. Overall, our results indicate that observed trade-offs in life history traits between the two gall former species are likely a result of independent adaptations in response to different environments as opposed to the amplified expression of within species intrinsic tradeoffs.

Speciation in Nearctic oak gall wasps is frequently correlated with changes in host plant, host organ, or both.

Quantifying the frequency of shifts to new host plants within diverse clades of specialist herbivorous insects is critically important to understand whether and how host shifts contribute to the origin of species. Oak gall wasps (Hymenoptera: Cynipidae: Cynipini) comprise a tribe of ∼1000 species of phytophagous insects that induce gall formation on various organs of trees in the family Fagacae-primarily the oaks (genus Quercus; ∼435 sp.). The association of oak gall wasps with oaks is ancient (∼50 my), and most oak species are galled by one or more gall wasp species. Despite the diversity of both gall wasp species and their plant associations, previous phylogenetic work has not identified the strong signal of host plant shifting among oak gall wasps that has been found in other phytophagous insect systems. However, most emphasis has been on the Western Palearctic and not the Nearctic where both oaks and oak gall wasps are considerably more species rich. We collected 86 species of Nearctic oak gall wasps from most of the major clades of Nearctic oaks and sequenced >1000 Ultraconserved Elements (UCEs) and flanking sequences to infer wasp phylogenies. We assessed the relationships of Nearctic gall wasps to one another and, by leveraging previously published UCE data, to the Palearctic fauna. We then used phylogenies to infer historical patterns of shifts among host tree species and tree organs. Our results indicate that oak gall wasps have moved between the Palearctic and Nearctic at least four times, that some Palearctic wasp clades have their proximate origin in the Nearctic, and that gall wasps have shifted within and between oak tree sections, subsections, and organs considerably more often than previous data have suggested. Given that host shifts have been demonstrated to drive reproductive isolation between host-associated populations in other phytophagous insects, our analyses of Nearctic gall wasps suggest that host shifts are key drivers of speciation in this clade, especially in hotspots of oak diversity. Although formal assessment of this hypothesis requires further study, two putatively oligophagous gall wasp species in our dataset show signals of host-associated genetic differentiation unconfounded by geographic distance, suggestive of barriers to gene flow associated with the use of alternative host plants.

The Build-Up of Population Genetic Divergence along the Speciation Continuum during a Recent Adaptive Radiation of Rhagoletis Flies.

New species form through the evolution of genetic barriers to gene flow between previously interbreeding populations. The understanding of how speciation proceeds is hampered by our inability to follow cases of incipient speciation through time. Comparative approaches examining different diverging taxa may offer limited inferences, unless they fulfill criteria that make the comparisons relevant. Here, we test for those criteria in a recent adaptive radiation of the Rhagoletis pomonella species group (RPSG) hypothesized to have diverged in sympatry via adaptation to different host fruits. We use a large-scale population genetic survey of 1568 flies across 33 populations to: (1) detect on-going hybridization, (2) determine whether the RPSG is derived from the same proximate ancestor, and (3) examine patterns of clustering and differentiation among sympatric populations. We find that divergence of each in-group RPSG taxon is occurring under current gene flow, that the derived members are nested within the large pool of genetic variation present in hawthorn-infesting populations of R. pomonella, and that sympatric population pairs differ markedly in their degree of genotypic clustering and differentiation across loci. We conclude that the RPSG provides a particularly robust opportunity to make direct comparisons to test hypotheses about how ecological speciation proceeds despite on-going gene flow.

Testing the potential contribution of Wolbachia to speciation when cytoplasmic incompatibility becomes associated with host-related reproductive isolation.

Endosymbiont-induced cytoplasmic incompatibility (CI) may play an important role in arthropod speciation. However, whether CI consistently becomes associated or coupled with other host-related forms of reproductive isolation (RI) to impede the transfer of endosymbionts between hybridizing populations and further the divergence process remains an open question. Here, we show that varying degrees of pre- and postmating RI exist among allopatric populations of two interbreeding cherry-infesting tephritid fruit flies (Rhagoletis cingulata and R. indifferens) across North America. These flies display allochronic and sexual isolation among populations, as well as unidirectional reductions in egg hatch in hybrid crosses involving southwestern USA males. All populations are infected by a Wolbachia strain, wCin2, whereas a second strain, wCin3, only co-infects flies from the southwest USA and Mexico. Strain wCin3 is associated with a unique mitochondrial DNA haplotype and unidirectional postmating RI, implicating the strain as the cause of CI. When coupled with nonendosymbiont RI barriers, we estimate the strength of CI associated with wCin3 would not prevent the strain from introgressing from infected southwestern to uninfected populations elsewhere in the USA if populations were to come into secondary contact and hybridize. In contrast, cytoplasmic-nuclear coupling may impede the transfer of wCin3 if Mexican and USA populations were to come into contact. We discuss our results in the context of the general paucity of examples demonstrating stable Wolbachia hybrid zones and whether the spread of Wolbachia among taxa can be constrained in natural hybrid zones long enough for the endosymbiont to participate in speciation.

The Arthropod Associates of 155 North American Cynipid Oak Galls.

The identities of most arthropod associates of cynipid-induced oak galls in the western Palearctic are generally known. However, a comprehensive accounting of associates has been performed for only a small number of the galls induced by the estimated 700 species of cynipid gall wasps in the Nearctic. This gap in knowledge stymies many potential studies of diversity, coevolution, and community ecology, for which oak gall systems are otherwise ideal models. We report rearing records of insects and other arthropods from more than 527,306 individual galls representing 201 different oak gall types collected from 32 oak tree species in North America. Of the 201 gall types collected, 155 produced one or more arthropods. A total of 151,075 arthropods were found in association with these 155 gall types, and of these 61,044 (40.4%) were gall wasps while 90,031 (59.6%) were other arthropods. We identified all arthropods to superfamily, family, or, where possible, to genus. We provide raw numbers and summaries of collections, alongside notes on natural history, ecology, and previously published associations for each taxon. For eight common gall-associated genera (Synergus, Ceroptres, Euceroptres, Ormyrus, Torymus, Eurytoma, Sycophila, and Euderus), we also connect rearing records to gall wasp phylogeny, geography, and ecology -including host tree and gall location (host organ), and their co-occurrence with other insect genera. Though the diversity of gall wasps and the large size of these communities is such that many Nearctic oak gall-associated insects still remain undescribed, this large collection and identification effort should facilitate the testing of new and varied ecological and evolutionary hypotheses in Nearctic oak galls.

Temporal resource partitioning mitigates interspecific competition and promotes coexistence among insect parasites.

A key to understanding life's great diversity is discerning how competing organisms divide limiting resources to coexist in diverse communities. While temporal resource partitioning has long been hypothesized to reduce the negative effects of interspecific competition, empirical evidence suggests that time may not often be an axis along which animal species routinely subdivide resources. Here, we present evidence to the contrary in the world's most biodiverse group of animals: insect parasites (parasitoids). Specifically, we conducted a meta-analysis of 64 studies from 41 publications to determine if temporal resource partitioning via variation in the timing of a key life-history trait, egg deposition (oviposition), mitigates interspecific competition between species pairs sharing the same insect host. When competing species were manipulated to oviposit at (or near) the same time in or on a single host in the laboratory, competition was common, and one species was typically inherently superior (i.e. survived to adulthood a greater proportion of the time). In most cases, however, the inferior competitor could gain a survivorship advantage by ovipositing earlier (or in a smaller number of cases later) into shared hosts. Moreover, this positive (or in a few cases negative) priority advantage gained by the inferior competitor increased as the interval between oviposition times became greater. The results from manipulative experiments were also correlated with patterns of life-history timing and demography in nature: the more inherently competitively inferior a species was in the laboratory, the greater the interval between oviposition times of taxa in co-occurring populations. Additionally, the larger the interval between oviposition times of competing taxa, the more abundant the inferior species was in populations where competitors were known to coexist. Overall, our findings suggest that temporal resource partitioning via variation in oviposition timing may help to facilitate species coexistence and structures diverse insect communities by altering demographic measures of species success. We argue that the lack of evidence for a more prominent role of temporal resource partitioning in promoting species coexistence may reflect taxonomic differences, with a bias towards larger-sized animals. For smaller species like parasitic insects that are specialized to attack one or a group of closely related hosts, have short adult lifespans and discrete generation times, compete directly for limited resources in small, closed arenas and have life histories constrained by host phenology, temporal resource subdivision via variation in life history may play a critical role in allowing species to coexist by alleviating the negative effects of interspecific competition.

Trade-off between fecundity and survival generates stabilizing selection on gall size.

Complex interactions within multitrophic communities are fundamental to the evolution of individual species that reside within them. One common outcome of species interactions are fitness trade-offs, where traits adaptive in some circumstances are maladaptive in others. Here, we identify a fitness trade-off between fecundity and survival in the cynipid wasp Callirhytis quercusbatatoides that induces multichambered galls on the stem of its host plant Quercus virginiana. We first quantified this trade-off in natural populations by documenting two relationships: a positive association between the trait gall size and fecundity, as larger galls contain more offspring, and a negative association between gall size and survival, as larger galls are attacked by birds at a higher rate. Next, we performed a field-based experimental evolution study where birds were excluded from the entire canopy of 11 large host trees for five years. As a result of the five-year release from avian predators, we observed a significant shift to larger galls per tree. Overall, our study demonstrates how two opposing forces of selection can generate stabilizing selection on a critical phenotypic trait in wild populations, and how traits can evolve rapidly in the predicted direction when conditions change.