Phylogeny-based comparative methods question the adaptive nature of sporophytic specializations in mosses

Abstract

Adaptive evolution has often been proposed to explain correlations between habitats and certain phenotypes. In mosses, a high frequency of species with specialized sporophytic traits in exposed or epiphytic habitats was, already 100 years ago, suggested as due to adaptation. We tested this hypothesis by contrasting phylogenetic and morphological data from two moss families, Neckeraceae and Lembophyllaceae, both of which show parallel shifts to a specialized morphology and to exposed epiphytic or epilithic habitats. Phylogeny-based tests for correlated evolution revealed that evolution of four sporophytic traits is correlated with a habitat shift. For three of them, evolutionary rates of dual character-state changes suggest that habitat shifts appear prior to changes in morphology. This suggests that they could have evolved as adaptations to new habitats. Regarding the fourth correlated trait the specialized morphology had already evolved before the habitat shift. In addition, several other specialized "epiphytic" traits show no correlation with a habitat shift. Besides adaptive diversification, other processes thus also affect the match between phenotype and environment. Several potential factors such as complex genetic and developmental pathways yielding the same phenotypes, differences in strength of selection, or constraints in phenotypic evolution may lead to an inability of phylogeny-based comparative methods to detect potential adaptations.

Figure 1. Sporophyte structure in Neckeraceae.

Example of a perfect and a specialized sporophyte structure in Neckeraceae. a) Homalia trichomanoides gametophyte (i) and sporophytes (ii) with long setas and slightly inclined capsules; b) SEM view of well-developed hypnalean peristome in H. trichomanoides. c) Neckera pennata gametophyte (i) and sporophytes (ii) that have short setas immersed in perichaetial leaves and upright capsules; d) SEM view of reduced peristome in N. pennata. Pictures reprinted with permission of M. S. Ignatov and E. Ignatova.

Figure 2. Ancestral character state reconstruction for habitat preference and four morphological traits.

Ancestral character state reconstruction for habitat preference and four morphological traits that evolution may correlate with the habitat shifts among Neckeraceae and Lembophyllaceae. The color of the branches in the inferred Bayesian topology represents two states of the habitat: on soil/unexposed (light gray) and epiphytic/exposed (for branches with probability >0.95 = black). Branches with probability >0.90 but <0.95 for epiphytic/exposed habitats are with dark gray color. Probabilities for morphological ancestral character state are shown as pie diagrams in the nodes. BayesFactor (BF) support for epiphytic/exposed habitat preference is shown below branches. For morphological traits BF for a derived character state is indicated with color of pie diagrams: BF <2 light gray, BF >2 dark gray; and BF >5 with black (see Table 1). Pie diagrams along branches are in the same order as in the legend showing their character states (a–d). Character states for terminals are stated before the taxon name. Dash (−) indicates missing or inapplicable data. Nodes A–E with show lineages with shifts to epiphytic or other exposed habitats.