Long-distance pollen dispersal during recent colonization favors a rapid but partial recovery of genetic diversity in Picea sitchensis.

Tree species in the northern hemisphere are currently subject to rapid anthropogenic climate change and are shifting their ranges in response. This prompts questions about the mechanisms allowing tree populations to respond quickly to selection pressures when establishing into new areas. Focusing on the northern expanding range edge of Picea sitchensis, a widespread conifer of western North America, we ask how genetic structure and diversity develop during colonization, and assess the role of demographic history in shaping the evolutionary trajectory of an establishing population. We combined 500 yr of tree-ring and genotyping-by-sequencing data in 639 trees at the expansion front on the Kodiak Archipelago. We show that alleles accumulated rapidly during an increase in recruitment rate in the early 1700s. A shift from foreign to local pollen flow subsequently homogenized genetic structure at the expansion front. Taking advantage of the exceptional longevity of conifers, we highlight the major role of long-distance pollen dispersal in the rapid but incomplete recovery of genetic diversity during the initial stages of colonization. We also warn that slow initial population growth as well as long-lasting dominance of local gene flow by early founders could increase evolutionary load under a rapidly changing climate.

Selection and gene flow shape genomic islands that control floral guides.

Genomes of closely-related species or populations often display localized regions of enhanced relative sequence divergence, termed genomic islands. It has been proposed that these islands arise through selective sweeps and/or barriers to gene flow. Here, we genetically dissect a genomic island that controls flower color pattern differences between two subspecies of Antirrhinum majus, A.m.striatum and A.m.pseudomajus, and relate it to clinal variation across a natural hybrid zone. We show that selective sweeps likely raised relative divergence at two tightly-linked MYB-like transcription factors, leading to distinct flower patterns in the two subspecies. The two patterns provide alternate floral guides and create a strong barrier to gene flow where populations come into contact. This barrier affects the selected flower color genes and tightly-linked loci, but does not extend outside of this domain, allowing gene flow to lower relative divergence for the rest of the chromosome. Thus, both selective sweeps and barriers to gene flow play a role in shaping genomic islands: sweeps cause elevation in relative divergence, while heterogeneous gene flow flattens the surrounding "sea," making the island of divergence stand out. By showing how selective sweeps establish alternative adaptive phenotypes that lead to barriers to gene flow, our study sheds light on possible mechanisms leading to reproductive isolation and speciation.

Exploring Approximate Bayesian Computation for inferring recent demographic history with genomic markers in nonmodel species.

Approximate Bayesian computation (ABC) is widely used to infer demographic history of populations and species using DNA markers. Genomic markers can now be developed for nonmodel species using reduced representation library (RRL) sequencing methods that select a fraction of the genome using targeted sequence capture or restriction enzymes (genotyping-by-sequencing, GBS). We explored the influence of marker number and length, knowledge of gametic phase, and tradeoffs between sample size and sequencing depth on the quality of demographic inferences performed with ABC. We focused on two-population models of recent spatial expansion with varying numbers of unknown parameters. Performing ABC on simulated data sets with known parameter values, we found that the timing of a recent spatial expansion event could be precisely estimated in a three-parameter model. Taking into account uncertainty in parameters such as initial population size and migration rate collectively decreased the precision of inferences dramatically. Phasing haplotypes did not improve results, regardless of sequence length. Numerous short sequences were as valuable as fewer, longer sequences, and performed best when a large sample size was sequenced at low individual depth, even when sequencing errors were added. ABC results were similar to results obtained with an alternative method based on the site frequency spectrum (SFS) when performed with unphased GBS-type markers. We conclude that unphased GBS-type data sets can be sufficient to precisely infer simple demographic models, and discuss possible improvements for the use of ABC with genomic data.