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.

Seed predation selects for reproductive variability and synchrony in perennial plants.

Annually variable and synchronous seed production by plant populations, or masting, is a widespread reproductive strategy in long-lived plants. Masting is thought to be selectively beneficial because interannual variability and synchrony increase the fitness of plants through economies of scale that decrease the cost of reproduction per surviving offspring. Predator satiation is believed to be a key economy of scale, but whether it can drive phenotypic evolution for masting in plants has been rarely explored. We used data from seven plant species (Quercus humilis, Quercus ilex, Quercus rubra, Quercus alba, Quercus montana, Sorbus aucuparia and Pinus pinea) to determine whether predispersal seed predation selects for plant phenotypes that mast. Predation selected for interannual variability in Mediterranean oaks (Q. humilis and Q. ilex), for synchrony in Q. rubra, and for both interannual variability and reproductive synchrony in S. aucuparia and P. pinea. Predation never selected for negative temporal autocorrelation of seed production. Predation by invertebrates appears to select for only some aspects of masting, most importantly high coefficient of variation, supporting individual-level benefits of the population-level phenomenon of mast seeding. Determining the selective benefits of masting is complex because of interactions with other seed predators, which may impose contradictory selective pressures.

Search for polyoma-, herpes-, and bornaviruses in squirrels of the family Sciuridae.

BACKGROUND: Squirrels (family Sciuridae) are globally distributed members of the order Rodentia with wildlife occurrence in indigenous and non-indigenous regions (as invasive species) and frequent presence in zoological gardens and other holdings. Multiple species introductions, strong inter-species competition as well as the recent discovery of a novel zoonotic bornavirus resulted in increased research interest on squirrel pathogens. Therefore we aimed to test a variety of squirrel species for representatives of three virus families. METHODS: Several species of the squirrel subfamilies Sciurinae, Callosciurinae and Xerinae were tested for the presence of polyomaviruses (PyVs; family Polyomaviridae) and herpesviruses (HVs; family Herpesviridae), using generic nested polymerase chain reaction (PCR) with specificity for the PyV VP1 gene and the HV DNA polymerase (DPOL) gene, respectively. Selected animals were tested for the presence of bornaviruses (family Bornaviridae), using both a broad-range orthobornavirus- and a variegated squirrel bornavirus 1 (VSBV-1)-specific reverse transcription-quantitative PCR (RT-qPCR). RESULTS: In addition to previously detected bornavirus RNA-positive squirrels no more animals tested positive in this study, but four novel PyVs, four novel betaherpesviruses (BHVs) and six novel gammaherpesviruses (GHVs) were identified. For three PyVs, complete genomes could be amplified with long-distance PCR (LD-PCR). Splice sites of the PyV genomes were predicted in silico for large T antigen, small T antigen, and VP2 coding sequences, and experimentally confirmed in Vero and NIH/3T3 cells. Attempts to extend the HV DPOL sequences in upstream direction resulted in contiguous sequences of around 3.3 kilobase pairs for one BHV and two GHVs. Phylogenetic analysis allocated the novel squirrel PyVs to the genera Alpha- and Betapolyomavirus, the BHVs to the genus Muromegalovirus, and the GHVs to the genera Rhadinovirus and Macavirus. CONCLUSIONS: This is the first report on molecular identification and sequence characterization of PyVs and HVs and the detection of bornavirus coinfections with PyVs or HVs in two squirrel species. Multiple detection of PyVs and HVs in certain squirrel species exclusively indicate their potential host association to a single squirrel species. The novel PyVs and HVs might serve for a better understanding of virus evolution in invading host species in the future.

Does masting scale with plant size? High reproductive variability and low synchrony in small and unproductive individuals.

BACKGROUND AND AIMS: In a range of plant species, the distribution of individual mean fecundity is skewed and dominated by a few highly fecund individuals. Larger plants produce greater seed crops, but the exact nature of the relationship between size and reproductive patterns is poorly understood. This is especially clear in plants that reproduce by exhibiting synchronized quasi-periodic variation in fruit production, a process called masting. METHODS: We investigated covariation of plant size and fecundity with individual-plant-level masting patterns and seed predation in 12 mast-seeding species: Pinus pinea, Astragalus scaphoides, Sorbus aucuparia, Quercus ilex, Q. humilis, Q. rubra, Q. alba, Q. montana, Chionochloa pallens, C. macra, Celmisia lyallii and Phormium tenax. KEY RESULTS: Fecundity was non-linearly related to masting patterns. Small and unproductive plants frequently failed to produce any seeds, which elevated their annual variation and decreased synchrony. Above a low fecundity threshold, plants had similar variability and synchrony, regardless of their size and productivity. CONCLUSIONS: Our study shows that within-species variation in masting patterns is correlated with variation in fecundity, which in turn is related to plant size. Low synchrony of low-fertility plants shows that the failure years were idiosyncratic to each small plant, which in turn implies that the small plants fail to reproduce because of plant-specific factors (e.g. internal resource limits). Thus, the behaviour of these sub-producers is apparently the result of trade-offs in resource allocation and environmental limits with which the small plants cannot cope. Plant size and especially fecundity and propensity for mast failure years play a major role in determining the variability and synchrony of reproduction in plants.

Correlated seed failure as an environmental veto to synchronize reproduction of masting plants.

Variable, synchronized seed production, called masting, is a widespread reproductive strategy in plants. Resource dynamics, pollination success, and, as described here, environmental veto are possible proximate mechanisms driving masting. We explored the environmental veto hypothesis, which assumes that reproductive synchrony is driven by external factors preventing reproduction in some years, by extending the resource budget model of masting with correlated reproductive failure. We ran this model across its parameter space to explore how key parameters interact to drive seeding dynamics. Next, we parameterized the model based on 16 yr of seed production data for populations of red (Quercus rubra) and white (Quercus alba) oaks. We used these empirical models to simulate seeding dynamics, and compared simulated time series with patterns observed in the field. Simulations showed that resource dynamics and reproduction failure can produce masting even in the absence of pollen coupling. In concordance with this, in both oaks, among-year variation in resource gain and correlated reproductive failure were necessary and sufficient to reproduce masting, whereas pollen coupling, although present, was not necessary. Reproductive failure caused by environmental veto may drive large-scale synchronization without density-dependent pollen limitation. Reproduction-inhibiting weather events are prevalent in ecosystems, making described mechanisms likely to operate in many systems.

Rapid aggregative and reproductive responses of weevils to masting of North American oaks counteract predator satiation.

The predator satiation hypothesis posits that masting helps plants escape seed predation through starvation of predators in lean years, followed by satiation of predators in mast years. Importantly, successful satiation requires sufficiently delayed bottom-up effects of seed availability on seed consumers. However, some seed consumers may be capable of quick aggregative and reproductive responses to masting, which may jeopardize positive density dependence of seed survival. We used a 17-yr data set on seed production and insect (Curculio weevils) infestation of three North American oaks species (northern red Quercus rubra, white Q. alba, and chestnut oak Q. montana) to test predictions of the predation satiation hypothesis. Furthermore, we tested for the unlagged numerical response of Curculio to acorn production. We found that masting results in a bottom-up effect on the insect population; both through increased reproductive output and aggregation at seed-rich trees. Consequently, mast seeding in two out of three studied oaks (white and chestnut oak) did not help to escape insect seed predation, whereas, in the red oak, the escape depended on the synchronization of mast crops within the population. Bottom-up effects of masting on seed consumer populations are assumed to be delayed, and therefore to have negligible effects on seed survival in mast years. Our research suggests that insect populations may be able to mount rapid reproductive and aggregative responses when seed availability increases, possibly hindering satiation effects of masting. Many insect species are able to quickly benefit from pulsed resources, making mechanisms described here potentially relevant in many other systems.

Scatterhoarding rodents favor higher predation risks for cache sites: The potential for predators to influence the seed dispersal process.

Scatterhoarding rodents often place caches in the open where pilferage rates are reduced, suggesting that they tradeoff higher risks of predation for more secure cache sites. We tested this hypothesis in two study systems by measuring predation risks inferred from measures of giving-up densities (GUDs) at known cache sites and other sites for comparison. Rodent GUDs were measured with small trays containing 3 L of fine sand mixed with sunflower seeds. In the first experiment, we relied on a 2-year seed dispersal study in a natural forest to identify caches of eastern gray squirrels (Sciurus carolinensis) and then measured GUDs at: (i) these caches; (ii) comparable points along logs and rocks where rodent activity was assumed highest; and (iii) a set of random points. We found that GUDs and, presumably, predation risks, were higher at both cache and random points than those with cover. At the second site, we measured GUDs of eastern gray squirrels in an open park system and found that GUDs were consistently lowest at the base of the tree compared to more open sites, where previous studies show caching by squirrels to be highest and pilferage rates by naïve competitors to be lowest. These results confirm that predation risks can influence scatterhoarding decisions but that they are also highly context dependent, and that the landscape of fear, now so well documented in the literature, could potentially shape the temporal and spatial patterns of seedling establishment and forest regeneration in systems where scatterhoarding is common.