Stochastic processes and changes in evolutionary rate are associated with diversification in a lineage of tropical hard pines (Pinus).

The study of the patterns of polymorphism and molecular evolution among closely related species is key to understanding the evolutionary forces involved in the diversification of lineages. This point is a big challenge in species with slow evolutionary rates, long life cycles, and ancient, shared polymorphisms such as conifers. Under the premise of divergence in a stepwise migration process, we expect clinal geographical patterns of purifying selection efficiency, and genetic structure related to latitude or longitude. If migration is accompanied by changes in the environment, we could further expect a role of positive selection in driving species divergence. Here, we infer patterns of polymorphism, efficiency of purifying selection, and molecular evolution using a dataset of 161 nuclear genes (∼71 Kb) in a lineage of hard pines from North America, the Caribbean, Mexico, and Central America presumed to have migrated from North America toward lower latitudes with tropical conditions. Under the premise of differences in selective pressures, we also look for possible signals of positive selection. To test our hypothesis, first we estimated different indices to infer patterns of polymorphism and efficiency of purifying selection (Ka, Ks, Ka/Ks, dN, dS, dN/dS, and dxy) and compared these metrics across five clades. Also, we investigated possible clinal patterns in these indices and morphological traits (needle length and cone length). Then we inferred genetic structure and environmental differences among species to test for possible signals of positive selection using phylogenetic methods in specific clades. We found differences among clades using Ka, Ks, and Ka/Ks with a relaxation of purifying selection, especially in the Elliotti and Patula clades. We also found environmental differences related to geographic distance, and among clades suggesting differences in selective pressures. The indices Ks, dxy, and needle length had relationships with geography but not ovulate cone length. Finally, we found that most analyzed genes are under purifying selection, but there was an exception of faster evolutionary rate in some pine species, suggesting the possible action of positive selection in divergence. Our study indicated that stochastic processes have played a key role in the diversification of the group, with a possible input of positive selection in pines from Mexico and Central America.

Non-adaptive evolutionary processes governed the diversification of a temperate conifer lineage after its migration into the tropics.

Constructing phylogenetic relationships among closely related species is a recurrent challenge in evolutionary biology, particularly for long-lived taxa with large effective population sizes and uncomplete reproductive isolation, like conifers. Conifers further have slow evolutionary rates, which raises the question of whether adaptive or non/adaptive processes were predominantly involved when they rapidly diversified after migrating from temperate regions into the tropical mountains. Indeed, fine-scale phylogenetic relationships within several conifer genus remain under debate. Here, we studied the phylogenetic relationships of endemic firs (Abies, Pinaceae) discontinuously distributed in the montane forests from the Southwestern United States to Guatemala, and addressed several hypotheses related to adaptive and non-adaptive radiations. We derived over 80 K SNPs from genotyping by sequencing (GBS) for 45 individuals of nine Mesoamerican species to perform phylogenetic analyses. Both Maximum Likelihood and quartets-inference phylogenies resulted in a well-resolved topology, showing a single fir lineage divided in four subgroups that coincided with the main mountain ranges of Mesoamerica; thus having important taxonomic implications. Such subdivision fitted a North-South isolation by distance framework, in which non-adaptive allopatric processes seemed the rule. Interestingly, several reticulations were observed within subgroups, especially in the central-south region, which may explain past difficulties for generating infrageneric phylogenies. Further evidence for non-adaptive processes was obtained from analyses of 21 candidate-gene regions, which exhibited diminishing values of πa/πs and Ka/Ks with latitude, thus indicating reduced efficiency of purifying selection towards the Equator. Our study indicates that non-adaptive allopatric processes may be key generators of species diversity and endemism in the tropics.