Genetic differentiation and evolution of broad-leaved evergreen shrub and tree varieties of Daphniphyllum macropodum (Daphniphyllaceae)

Abstract

Tree form evolution is an important ecological specialization for woody species, but its evolutionary process with adaptation is poorly understood, especially on the microevolutionary scale. Daphniphyllum macropodum comprises two varieties: a tree variety growing in a warm temperate climate with light snowfall and a shrub variety growing in a cool temperate climate with heavy snowfall in Japan. Chloroplast DNA variations and genome-wide single-nucleotide polymorphisms across D. macropodum populations and D. teijsmannii as an outgroup were used to reveal the evolutionary process of the shrub variety. Population genetic analysis indicated that the two varieties diverged but were weakly differentiated. Approximate Bayesian computation analysis supported a scenario that assumed migration between the tree variety and the southern populations of the shrub variety. We found migration between the two varieties where the distributions of the two varieties are in contact, and it is concordant with higher tree height in the southern populations of the shrub variety than the northern populations. The genetic divergence between the two varieties was associated with snowfall. The heavy snowfall climate is considered to have developed since the middle Quaternary in this region. The estimated divergence time between the two varieties suggests that the evolution of the two varieties may be concordant with such paleoclimatic change.

Fig. 1. Distributions of analyzed populations and chloroplast DNA haplotypes, genetic clusters elucidated by sNMF, and approximate maximum tree height of the population.

a Small letters indicate population codes corresponding to those in Table 1. Pie charts indicate frequencies of chloroplast DNA haplotypes, and the green and blue outer circles of the pie charts indicate Daphniphyllum macropodum var. macropodum and var. humile, respectively. A haplotype network is superimposed on the map. b Geographical distributions of ancestry for the two varieties when K = 4, the optimal number of clusters supported by the cross-entropy criterion. Snow depth is shown only for Japan, which is modified data from Japan Meteorological Agency (https://www.data.jma.go.jp/obd/stats/etrn/view/atlas.html). c Approximate maximum tree height of the population. d Distributions of ancestry when the number of clusters ranged from K = 2–5.

Fig. 2. Comparison of the three group divergence scenarios.

The four scenarios are no migration (NM), isolation with migration (IM), ancient migration (AM), and secondary contact (SC). M, Daphniphyllum macropodum var. macropodum; HS and HN, southern and northern D. macropodum var. humile, respectively. N, effective population size; T, event time; Nm_ij, number of migrants per generation from j to i (1, M; 2, HS; 3 HN). Direction of migration is forward in time. The period shown in light gray indicates that a migration is occurring.

Fig. 3. Genetic relationships among populations, constructed based on D_A distance using the neighbor-joining method.

Relationships a with and b without the outgroup species, Daphniphyllum teijsmannii. Bootstrap probabilities that were a 100% and b exceeded 80% based on 1000 replicates are shown above nodes. Populations codes are shown in Table 1. Red, green and blue are Daphniphyllum macropodum var. macropodum (M), southern (HS) and northern (HN) D. macropodum var. humile, respectively.

Fig. 4. Genetic relationships among individuals detected by principal component analysis (PCA).

M, Daphniphyllum macropodum var. macropodum; HS and HN, southern and northern D. macropodum var. humile, respectively. Proportions of variance explained for the two principal components were evaluated from the top 50 components.

Fig. 5. The effective population size and number of migrants per generation in the three island groups are denoted by circles and arrows, respectively, in the best scenario (isolation with migration, IM).

The sizes of the circles and arrows are proportional to the value of the posterior mode of the parameter. The effective population sizes were at T₂ and T₀. Numbers indicate posterior mode with 95% highest posterior density. Direction of migration is forward in time. Photographs were obtained for each representative population. M, Daphniphyllum macropodum var. macropodum; HS and HN, southern and northern D. macropodum var. humile, respectively.