Dean A. Williams

Chloroplast and microsatellite DNA diversities reveal the introduction history of Brazilian peppertree (Schinus terebinthifolius) in Florida.

Brazilian peppertree (Schinus terebinthifolius) is a woody perennial that has invaded much of Florida. This native of northeastern Argentina, Paraguay, and Brazil was brought as an ornamental to both the west and east coasts of Florida at the end of the 19th century. It was recorded as an invader of natural areas in the 1950s, and has since extended its range to cover over 280 000 ha. Our goals were to understand the history of this invasion, as one step toward understanding why this exotic was so successful, and ultimately to improve development of biological control agents. We sampled plants from the native and exotic ranges, particularly Florida, and genotyped these individuals at nuclear and chloroplast loci. Nuclear microsatellite and cpDNA loci reveal strong genetic population structure consistent with limited dispersal in the introduced and native ranges. Bayesian clustering of microsatellite data separates the east and west coast plants in Florida into distinct populations. The two chloroplast haplotypes found in Florida are also concordant with this separation: one predominates on the east coast, the other on the west coast. Analysis of samples collected in South America shows that haplotypes as distinct as the two in Florida are unlikely to have come from a single source population. We conclude that the genetic evidence supports two introductions of Brazilian peppertree into Florida and extensive hybridization between them. The west coast genotype likely came from coastal Brazil at about 27° south, whereas the east coast genotype probably originated from another, as yet unidentified site. As a result of hybridization, the Florida population does not exhibit low genetic variation compared to populations in the native range, possibly increasing its ability to adapt to novel environments. Hybridization also has important consequences for the selection of biocontrol agents since it will not be possible to identify closely co‐adapted natural enemies in the native range, necessitating more extensive host testing.

Weak genetic structure indicates strong dispersal limits: a tale of two coral reef fish

The extent of dispersal by pelagic larvae in marine environments, including coral reefs, is central for understanding local population dynamics and designing sustainable marine reserves. We present here the first example of a clear stepping-stone genetic structure throughout the Caribbean basin for a common coral reef species, the French grunt (Haemulon flavolineatum). Analysis of microsatellite DNA markers indicated that French grunt population structure may be characterized by overlapping populations throughout the Caribbean, influenced by independent population dynamics but with no fixed geographical boundaries. In addition, different spatial genetic patterns were found in different oceanographic regions. A second species, the bluehead wrasse (Thalassoma bifasciatum), has a much longer pelagic larval duration than French grunts and showed no explicit spatial pattern of genetic variation. This finding is concordant with the hypothesis of a positive relationship between larval dispersal and duration in the plankton. While the magnitude of the genetic signal of population structure in French grunts was very low (FST≈0.003), the pattern of isolation-by-distance throughout the Caribbean indicated considerable population structure with important ecological and conservation significance.

Colonization patterns of the invasive Brazilian peppertree, Schinus terebinthifolius, in Florida.

Invasive species are believed to spread through a process of stratified dispersal consisting of short-distance diffusive spread around established foci and human mediated long-distance jumps. Brazilian peppertree (Schinus terebinthifolius), native to South America, was introduced twice as an ornamental plant into Florida, USA, just over 100 years ago. A previous study indicated that these two introductions were from genetically differentiated source populations in the native range. In this study, we took advantage of these contrasting genetic signatures to study the spatial spread of Brazilian peppertree across its entire range in Florida. A combination of spatial genetic and geostatistical analyses using chloroplast and nuclear microsatellite markers revealed evidence for both diffusive dispersal and long-distance jumps. Chloroplast DNA haplotype distributions and extensive bands of intra-specific hybridization revealed extensive dispersal by both introduced populations across the state. The strong genetic signature around the original introduction points, the presence of a general southeast to northwest genetic cline, and evidence for short-distance genetic spatial autocorrelation provided evidence of diffusive dispersal from an advancing front, probably by birds and small mammals. In the northernmost part of the range, there were patches having a high degree of ancestry from each introduction, suggesting long-distance jump dispersal, probably by the movement of humans. The evidence for extensive movement throughout the state suggests that Brazilian peppertree will be capable of rapidly recolonizing areas from which it has been eradicated. Concerted eradication efforts over large areas or the successful establishment of effective biocontrol agents over a wide area will be needed to suppress this species.

Brazilian peppertree (Schinus terebinthifolius) in Florida and South America: evidence of a possible niche shift driven by hybridization

Brazilian peppertree (Schinus terebinthifolius Raddi, Anacardiaceae) was introduced into Florida from South America in the 1800s and commercialized as an ornamental plant. Based on herbaria records and available literature, it began to escape cultivation and invade ruderal and natural habitats in the 1950s, and is now considered to be one of Florida’s most widespread and damaging invasive plants. Historical records and molecular evidence indicate that two genetic lineages of Brazilian peppertree were established in Florida, one in Miami on the east coast and a second near Punta Gorda on the west coast. Since arriving, the distributions of these two types have greatly expanded, and they have extensively hybridized. Principal component analysis and reciprocal niche fitting were used to test the equivalency of climatic niches of the Florida populations with the climatic niches of the two South American chloroplast haplotype groups which established in Florida. Both approaches indicated a significant shift in niches between the parental populations in the native range and the invasive populations in Florida. The models, however, closely predicted the areas of initial establishment. We hypothesize that (1) Brazilian peppertree was able to gain an initial foothold in Florida due to niche similarity and (2) the current dissimilarity in native and exotic niches is due to hybridization followed by rapid selection of genotypes adapted to Florida’s climate. In addition, to examine the potential consequence of the introduction of additional genetic diversity from the native range on invasion success, a niche model constructed with occurrences of all native genotypes was projected onto the continental United States. The result of this test indicated that under such an event, the potential invasive range would greatly expand to cover most of the southeastern USA. Our study suggests that multiple introductions from disjunct regions in the native range can facilitate invasion success.

Hybrid Vigor for the Invasive Exotic Brazilian Peppertree (Schinus terebinthifolius Raddi., Anacardiaceae) in Florida

How can successful invaders overcome reduced genetic variation via small founder population sizes to persist, thrive, and successfully adapt to a new set of environmental conditions? An expanding body of literature posits hybridization, both inter- and intraspecific, as a driver of the evolution of invasiveness via genetic processes. We studied Brazilian peppertree (Schinus terebinthifolius), a tree species native to South America that is a successful invader throughout Florida. The tree was introduced separately to the east and west coasts of Florida more than 100 years ago from genetically distinct source populations. We conducted a common garden experiment to compare the early life-stage performance of hybrids versus their progenitors. We hypothesized that hybrids would outperform their progenitors due to the positive genetic effects of intraspecific hybridization (i.e., hybrid vigor). Hybrid seeds germinated at higher rates than eastern seeds. Over the 8-mo experiment, a greater proportion of hybrid seedlings survived than did western seedlings, and hybrids attained greater biomass than the western types. The cumulative hybrid advantage of both seed germination and seedling survival led to the establishment of nearly 45% more hybrid seedlings versus either progenitor. Documenting fitness advantages for hybrids over their progenitors is a requisite finding to consider hybridization as a factor in the success of invasive species.

The Effect of Genetic and Environmental Variation on Metabolic Gene Expression

What is the relationship between genetic or environmental variation and the variation in messenger RNA (mRNA) expression? To address this, microarrays were used to examine the effect of genetic and environmental variation on cardiac mRNA expression for metabolic genes in three groups of Fundulus heteroclitus: (i) individuals sampled in the field (field), (ii) field individuals acclimated for 6 months to laboratory conditions (acclimated), or (iii) individuals bred for 10 successive generations in a laboratory environment (G10). The G10 individuals have significantly less genetic variation than individuals obtained in the field and had a significantly lower variation in mRNA expression across all genes in comparison to the other two groups (P = 0.001). When examining the gene specific variation, 22 genes had variation in expression that was significantly different among groups with lower variation in G10 individuals than in acclimated individuals. Additionally, there were fewer genes with significant differences in expression among G10 individuals vs. either acclimated or field individuals: 66 genes have statistically different levels of expression vs. 107 or 97 for acclimated or field groups. Based on the permutation of the data, these differences in the number of genes with significant differences among individuals within a group are unlikely to occur by chance (P < 0.01). Surprisingly, variation in mRNA expression in field individuals is lower than in acclimated individuals. Relative to the variation among individual within a group, few genes have significant differences in expression among groups (seven, 2.3%) and none of these are different between acclimated and field individuals. The results support the concept that genetic variation affects variation in mRNA expression and also suggests that temporal environmental variation associated with estuarine environments does not increase the variation among individuals or add to the differences among groups.

TERRITORIALITY AND NEIGHBOR ASSESSMENT IN BROWN JAYS (CYANOCORAX MORIO) IN COSTA RICA

Abstract Defense of group-held resources is a common and widely accepted function of territorial interactions between neighboring groups. In addition, territorial interactions could provide opportunities to assess members of neighboring groups and reproductive opportunities there, or to solidify status in the home group. We studied group-level characteristics and individual participation in territorial encounters in the cooperatively breeding Brown Jay (Cyanocorax morio). Intergroup encounters at stable territory boundaries include both aggressive and affiliative behavior, which suggests that a territorial encounter could function as both a resource defense mechanism and as an arena for social interactions. Territory characteristics that increase the probability of contact between groups (long boundaries, large combined group size, and home range overlap) explain much of the variation in frequency of territorial encounters. Male-biased dispersal was more common to neighboring groups with long boundaries, supporting the idea that frequent interactions between neighbors facilitate dispersal. Females usually inherit breeding positions on their natal territories, and participation in intergroup encounters by females does not vary with age or breeding status. In addition to defending group resources, females on their natal territories could be defending their positions in the breeding queue. Immigrant females are not likely to breed successfully, or to disperse again, and they participated less than expected. Participation by both natal and immigrant males varied by age; young males, at the ages when dispersal and intergroup forays are most likely, participated more than expected, whereas older males (≥4 years) participated less. That is consistent with the hypothesis that participation in intergroup encounters facilitates dispersal and improves integration into social groups. Because extragroup matings occur in this population, both breeding females and males could be assessing neighboring individuals for mating opportunities. Resource defense and social facilitation are not mutually exclusive hypotheses, and our observations suggest that both are important components of territorial encounters in Brown Jays.

Geographic Origins and Genetic Diversity of Air-Potato (Dioscorea bulbifera) in Florida

Abstract In Florida, air-potato is an invasive weed with high management priority, which may soon be targeted using classical biological control. This yam was introduced during the early 20th century by the United States Department of Agriculture (USDA) from areas throughout its extensive range. Our objectives were to characterize the genetic diversity of the invasive population in Florida and to identify the source regions of introduction. Authorities have often asserted the African provenance of the species in Florida, but our analyses, conducted using chloroplast markers, indicate that Florida air-potato is more similar to specimens examined from China than to those from Africa. Low intraspecific genetic diversity in Florida indicates that the invasive population was the result of at least two introductions becoming established in Florida. Nomenclature: Air-potato, Dioscorea bulbifera L Interpretive Summary: Two distinct, but genetically similar, chloroplast haplotypes were identified in the Florida population of the invasive yam vine, air-potato. Assuming no contribution of somatic mutation in the invasive population, these data are consistent with a minimum of two introductions into Florida. This study contributes baseline information regarding the diversity of air-potato before implementation of biological control in Florida. In the course of examining plant material to locate a putative source population, we characterized the genetic diversity of African air-potato, sampling six haplotypes on that continent. Three of the most prevalent African haplotypes were also geographically widespread, being found in both East Africa and West Africa. These three are also the most genetically distant from Florida and Chinese haplotypes, relative to other African haplotypes, as determined by parsimonious network analysis. A neighbor-joining analysis supported the relationships inferred in a statistical parsimony network. Our study did not find evidence that haplotypes were geographically structured in Africa. Despite a small number of microsatellite markers employed, this methodology confirmed the similarity of Chinese and Florida samples. Future work using a greater number of markers is expected to reveal greater intraspecific diversity, whereas further sampling in Asia and Oceania may localize Floridas source population to a regional, rather than a continental, level. Integrative taxonomic approaches are needed to synthesize morphological treatments of this species with more recent molecular studies, including the present work.

Calophya latiforceps , a New Species of Jumping Plant Lice (Hemiptera: Calophyidae) Associated with Schinus terebinthifolius (Anacardiaceae) in Brazil

ABSTRACT Brazilian peppertree, Schinus terebinthifolius Raddi, is a perennial woody plant native to Brazil, Argentina, and Paraguay that is recognized as one of the most invasive weeds in Florida. A new species of leaflet galling psyllid was discovered attacking Brazilian peppertree in Bahia, Brazil in March 2010. In this paper, a formal morphological description of the new psyllid Calophya latiforceps sp. nov. (Hemiptera: Calophyidae) is presented along with molecular evidence confirming new species designation. This previously unknown natural enemy may have potential as a biological control agent for the Brazilian peppertree.

HELPER EFFECTS ON OFFSPRING PRODUCTION IN COOPERATIVELY BREEDING BROWN JAYS (CYANOCORAX MORIO)

Abstract Most studies of cooperatively breeding species have revealed that indirect fitness gains from helping are lower than benefits gained from direct reproduction. Exceptions to this “best of a bad job” strategy are rare. Brown Jays (Cyanocorax morio) in Monteverde, Costa Rica, live in large groups (mean = 10 individuals) and have never been observed to breed as unaided pairs. Helpers provide a substantial percentage (70%) of all nestling feedings. Together, these observations suggest that helping may be crucial for reproductive success in this population. We used multivariate models to examine the effect of helpers on offspring production using a long-term data set. Data on nest-site success and brood reduction suggested that predation was the major cause of nesting failure. Nesting in an isolated tree was the major determinant of successful nestling production, and our data indicate that small groups (less than 9 individuals) may not be able to acquire or defend territories that contain suitable nesting sites. The number of juveniles (young surviving 30 days after leaving the nest) and yearlings was positively related to group size, even after removing groups that nested only in non-isolated trees. Small groups were also more likely than large groups to have total reproductive failure in a season. Helpers may increase juvenile survival by reducing predation, increasing juvenile condition, or providing learning opportunities for foraging and antipredator behaviors. Helpers on their natal territories receive some indirect benefits, though these are low compared with independent breeding. Immigrant male helpers may benefit primarily by gaining future breeding opportunities. Delayed benefits related to territory inheritance and dispersal coalitions may be the best explanation for helping in this population. Efectos de los Ayudantes sobre la Producción de Progenie en Cyanocorax morio, una Especie con Cría Cooperativa