Pollination Mode and Mating System Explain Patterns in Genetic Differentiation in Neotropical Plants

Abstract

We studied genetic diversity and differentiation patterns in Neotropical plants to address effects of life history traits (LHT) and ecological attributes based on an exhaustive literature survey. We used generalized linear mixed models (GLMMs) to test the effects as fixed and random factors of growth form, pollination and dispersal modes, mating and breeding systems, geographical range and habitat on patterns of genetic diversity (HS, HeS, π and h), inbreeding coefficient (FIS), allelic richness (AR) and differentiation among populations (FST) for both nuclear and chloroplast genomes. In addition, we used phylogenetic generalized least squares (pGLS) to account for phylogenetic independence on predictor variables and verify the robustness of the results from significant GLMMs. In general, GLMM revealed more significant relationships among LHTs and genetic patterns than pGLS. After accounting for phylogenetic independence (i.e., using pGLS), FST for nuclear microsatellites was significantly related to pollination mode, mating system and habitat. Plants specifically with outcrossing mating system had lower FST. Moreover, AR was significantly related to pollination mode and geographical range and HeS for nuclear dominant markers was significantly related to habitat. Our findings showed that different results might be retrieved when phylogenetic non-independence is taken into account and that LHTs and ecological attributes affect substantially the genetic pattern in Neotropical plants, hence may drive key evolutionary processes in plants.

Fig 1. Conceptual framework summarizing the traditional analyses and the advanced approach proposed here to account for random factors and phylogenetic signal across predictors.

Fig 2. Mean values and 95% confidence intervals in the posterior distribution of the GLMM and phylogenetic coefficients and standard errors of pGLS for F_ST for nuclear microsatellite markers.

(a) Growth form. (b) Dispersal mode. (c) Pollination mode. (d) Breeding system. (e) Breeding system phylogenetic coefficients. (f) Mating system phylogenetic coefficients. (g) Habitat phylogenetic coefficients. Values highlighted by an asterisk are significant (* 0.05<P<0.01, ** P< 0.01, ***P<0.000).

Fig 3. Mean values and 95% confidence intervals in the posterior distribution of the GLMM for F_IS retrieved from isozymes.

(a) Growth form. (b) Habitat. Values highlighted by an asterisk are significant (* 0.05<P<0.01). Note that the mean value in posterior distribution for herbs in (a) -1.16.

Fig 4. Mean values and 95% confidence intervals in the posterior distribution of the GLMM and phylogenetic coefficients and standard errors of pGLS for genetic diversity overall populations (He_S) for nuclear dominant markers.

(a) Habitat (b) Habitat phylogenetic coefficients. Values highlighted by an asterisk are significant (* 0.05<P<0.01, ** P< 0.01). Note that the mean value in posterior distribution for rainforests in (a) is -0.50.

Fig 5. Mean values and 95% confidence intervals in the posterior distribution of the GLMM for genetic diversity overall populations (He_S) for nuclear microsatellites.

(a) Growth form (b) Habitat. Values highlighted by an asterisk are significant (* 0.05<P<0.01, ** P< 0.01).

Fig 6. Mean values and 95% confidence intervals in the posterior distribution of the GLMM and phylogenetic coefficients and standard errors of pGLS for allelic richness (AR) for nuclear microsatellites.

(a) Pollination mode (b) Pollination mode phylogenetic coefficients (c) Geographical range phylogenetic coefficients. Values highlighted by an asterisk are significant (* 0.05<P<0.01, ** P< 0.01).

Fig 7. Phylogenetic super-tree of the Neotropical plants included in the analyses, obtained from Phylomatic using the internal master tree Phylomatic tree R20120829, with life-history traits and ecological attributes mapped.

Growth form (❅): Fuchsia = Epiphytes, Red = Herbs, Blue = Palms, Brown = Shrubs, Green = Trees. Dispersal mode (▼): Orange = autochory, Brown = mixed (mammals and birds), Green = bats, Magenta = birds, Black = hydrochory, Dark blue = mammals, Light green = wind. Pollination mode (◗): Black = beetles, Yellow = birds, Brown = wasps, Red = small bees, Dark blue = wind, Purple = bats, Light blue = butterflies, Magenta = moth, Dark green = large bees, Light orange = flies. Geographical range (❙❙): Black = widespread, Grey = narrow. Habitat (❁): Sand = desert, Red = seasonally dry forests, Black = rainforests, Light green = grasslands, Brown = mangroves, Orange = mixed (rainforests and seasonally dry forests), Blue = rocky fields, Pink = rocky savannas, purple = savannas, Grey = wetlands. Reproductive system (❃): Brown = hermaphrodite, Dark blue = monoecious, Magenta = dioecious. Mating system (✭): Dark green = mixed, Dark red = outcrossing.