Kenneth D. Whitney

Hybridization and the colonization of novel habitats by annual sunflowers

Although invasive plant species often have a hybrid ancestry, unambiguous evidence that hybridization has stimulated the evolution of invasive behaviors has been difficult to come by. Here, we briefly review how hybridization might contribute to the colonization of novel habitats, range expansions, and invasiveness and then describe work on hybrid sunflowers that forges a direct link between hybridization and ecological divergence. We first discuss the invasion of Texas by the common sunflower and show that the introgression of chromosomal segments from a locally adapted species may have facilitated range expansion. We then present evidence that the colonization of sand dune, desert floor, and salt marsh habitats by three hybrid sunflower species was made possible by selection on extreme or “transgressive” phenotypes generated by hybridization. This body of work corroborates earlier claims regarding the role of hybridization in adaptive evolution and provides an experimental and conceptual framework for ongoing studies in this area.

Adaptive Introgression of Herbivore Resistance Traits in the Weedy Sunflower Helianthus annuus

The role of hybridization in adaptive evolution is contentious. While many cases of adaptive trait introgression have been proposed, the relevant traits have rarely been identified, resulting in a lack of clear examples of this process. Here, we examine a purported case of adaptive introgression in which the annual sunflower Helianthus annuus annuus has captured alleles from a congener (Helianthus debilis) to form a stabilized hybrid, Helianthus annuus texanus. We tested the hypotheses that herbivore resistance traits have introgressed from H. debilis to H. annuus and have increased adaptation in the latter. In two common gardens, fitness (estimated by seed production) was on average 55% higher in H. a. texanus than in H. a. annuus. For H. a. texanus, three damage traits (of seven tested) differed significantly from the H. a. annuus parent in one or both sites and were shifted in the direction of the more resistant H. debilis. Natural selection favored H. a. \documentclass{aastex} \usepackage{amsbsy} \usepackage{amsfonts} \usepackage{amssymb} \usepackage{bm} \usepackage{mathrsfs} \usepackage{pifont} \usepackage{stmaryrd} \usepackage{textcomp} \usepackage{portland,xspace} \usepackage{amsmath,amsxtra} \usepackage[OT2,OT1]{fontenc} \newcommand\cyr{ \renewcommand\rmdefault{wncyr} \renewcommand\sfdefault{wncyss} \renewcommand\encodingdefault{OT2} \normalfont \selectfont} \DeclareTextFontCommand{\textcyr}{\cyr} \pagestyle{empty} \DeclareMathSizes{10}{9}{7}{6} \begin{document} \landscape

Seed dispersal by Ceratogymna hornbills in the Dja Reserve, Cameroon

annuus\times H.

Genome scan of hybridizing sunflowers from Texas (Helianthus annuus and H. debilis) reveals asymmetric patterns of introgression and small islands of genomic differentiation

\end{document} debilis BC1 hybrids (synthesized to mimic the ancestors of H. a. texanus) with H. debilis–like resistance to seed midges Neolasioptera helianthis and to receptacle/seed feeding Lepidoptera at one or both sites. Assuming similar herbivore pressures in the past, these results suggest that introgression of biotic resistance traits was important in the adaptation of H. annuus to central and southern Texas.

Does phylogeny matter? Assessing the impact of phylogenetic information in ecological meta‐analysis

Much thought has been given to the individual‐level traits that may make a species a successful colonizer. However, these traits have proven to be weak predictors of colonization success. Here, we test whether population‐level characteristics, specifically genetic diversity and population density, can influence colonization ability on a short‐term ecological timescale, independent of longer‐term effects on adaptive potential. Within experimentally manipulated populations of the weedy herb Arabidopsis thaliana, we found that increased genetic diversity increased colonization success measured as population‐level seedling emergence rates, biomass production, flowering duration, and reproduction. Additive and non‐additive effects contributed to these responses, suggesting that both individual genotypes (sampling effect) and positive interactions among genotypes (complementarity) contributed to increased colonization success. In contrast, manipulation of plant density had no effect on colonization success. The heightened ability of relatively genetically rich populations to colonize novel habitats, if a general phenomenon, may have important implications for predicting and controlling biological invasions.

A ROLE FOR NONADAPTIVE PROCESSES IN PLANT GENOME SIZE EVOLUTION

Seed dispersal is a process critical to the maintenance of tropical forests, yet little is known about the interactions of most dispersers with their communities. In the Dja Reserve, Cameroon, seed dispersal by the hornbills Cerato- gymna atrata, C. cylindricus and C. fistulator (Aves: Bucerotidae) was evaluated with respect to the taxonomic breadth of plants dispersed, location of seed deposition and effects on seed germination. Collectively, the three hornbill species consumed fruits from 59 tree and liana species, and likely provided dispersal for 56 of them. Hornbill-dispersed tree species composed 22% of the known tree flora of the site. Hornbill visit lengths, visit frequencies, and seed passage times indicated that few seeds were deposited beneath parent trees; in five hornbill/tree species pairings studied, 69-100% of the seeds ingested were deposited away from the parent trees. Germination trials showed that hornbill gut passage is gentle on seeds. Of 24 tree species tested, 23 germinated after passage by hornbills; of 17 planted with con- trols taken directly from trees, only four species showed evidence of inhibition of germination rate, while seven experienced unchanged germination rates and six experienced enhanced germination rates. Results suggested that Ceratogymna horn- bills rank among the most important seed dispersers found in Afrotropical forests, and they deserve increased conservation attention. Ceratogymna hornbills are likely to become increasingly important in forest regeneration as populations of larger mammalian seed dispersers (such as forest elephants and primates) diminish.

Hybridisation is associated with increased fecundity and size in invasive taxa: meta-analytic support for the hybridisation-invasion hypothesis.

Mechanisms underlying the dramatic patterns of genome size variation across the tree of life remain mysterious. Effective population size (Ne) has been proposed as a major driver of genome size: selection is expected to efficiently weed out deleterious mutations increasing genome size in lineages with large (but not small) Ne. Strong support for this model was claimed from a comparative analysis of Neu and genome size for ≈30 phylogenetically diverse species ranging from bacteria to vertebrates, but analyses at that scale have so far failed to account for phylogenetic nonindependence of species. In our reanalysis, accounting for phylogenetic history substantially altered the perceived strength of the relationship between Neu and genomic attributes: there were no statistically significant associations between Neu and gene number, intron size, intron number, the half-life of gene duplicates, transposon number, transposons as a fraction of the genome, or overall genome size. We conclude that current datasets do not support the hypothesis of a mechanistic connection between Ne and these genomic attributes, and we suggest that further progress requires larger datasets, phylogenetic comparative methods, more robust estimators of genetic drift, and a multivariate approach that accounts for correlations between putative explanatory variables.

INSECT SEED PREDATORS AS NOVEL AGENTS OF SELECTIONON FRUIT COLOR

Although the sexual transfer of genetic material between species (i.e. introgression) has been documented in many groups of plants and animals, genome‐wide patterns of introgression are poorly understood. Is most of the genome permeable to interspecific gene flow, or is introgression typically restricted to a handful of genomic regions? Here, we assess the genomic extent and direction of introgression between three sunflowers from the south‐central USA: the common sunflower, Helianthus annuus ssp. annuus; a near‐endemic to Texas, Helianthus debilis ssp. cucumerifolius; and their putative hybrid derivative, thought to have recently colonized Texas, H. annuus ssp. texanus. Analyses of variation at 88 genetically mapped microsatellite loci revealed that long‐term migration rates were high, genome‐wide and asymmetric, with higher migration rates from H. annuus texanus into the two parental taxa than vice versa. These results imply a longer history of intermittent contact between H. debilis and H. annuus than previously believed, and that H. annuus texanus may serve as a bridge for the transfer of alleles between its parental taxa. They also contradict recent theory suggesting that introgression should predominantly be in the direction of the colonizing species. As in previous studies of hybridizing sunflower species, regions of genetic differentiation appear small, whether estimated in terms of FST or unidirectional migration rates. Estimates of recent immigration and admixture were inconsistent, depending on the type of analysis. At the individual locus level, one marker showed striking asymmetry in migration rates, a pattern consistent with tight linkage to a Bateson–Dobzhansky–Muller incompatibility.