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

Abstract

Summary 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.

Genomic vulnerability to rapid climate warming in a tree species with a long generation time

“…This was to be expected, as juvenile trees at high elevation most likely reflect the first generation of adult progenitors at lower elevations, and thus have not yet undergone major long‐term demographic processes (e.g. genetic drift) that would reduce overall genetic diversity (Elleouet & Aitken, 2019). However, as a result of selection imposed by the changing climate, alleles beneficial under warmer and drier conditions compared with those the progenitors of high‐elevation juveniles experienced during their establishment are already found uphill at the colonisation front (Figure 3).…”

Using paleo-archives to safeguard biodiversity under climate change

“…These episodic climatic events govern rates and patterns of range expansion and contraction(12). Studies of tree populations, for example, reveal the importance of non-stationary Holocene climate variability and its interactions with long-distance dispersal, local demographic processes, and species life-history traits(56)(57)(58)(59). Moreover, Holocene records show population expansions and declines are not necessarily accompanied by changes in geographic distribution(60,61), as is often assumed in conservation assessments(62).…”

Recovery process of genetic diversity through seed and pollen immigration at the northernmost leading‐edge population of Fagus crenata

“…As a consequence, the Niseko population is currently recovering its genetic diversity by effective long‐distance pollen flow from foreign sources. Also, previous studies of marginal populations indicated rapid recovery of the genetic diversity by gene flow, but this recovery became saturated with population growth (Elleouet & Aitken, 2019; Lesser et al, 2013). Moreover, the recovery was incomplete due to a shift from foreign to local pollen flow (Elleouet & Aitken, 2019).…”

“…However, when the size and the number of reproductive individuals in the local population increases, local reproductive success increases and the proportion of immigrant genes will decrease in the future (Elleouet & Aitken, 2019; Sezen, Chazdon, & Holsinger, 2005, 2007). Lesser et al (2013) pointed out that the accumulation of alleles would be saturated when the population size grows to a certain number of individuals.…”