Trends in Morphological Evolution in Homobasidiomycetes Inferred Using Maximum Likelihood: A Comparison of Binary and Multistate Approaches

Abstract

The homobasidiomycetes is a diverse group of macrofungi that includes mushrooms, puffballs, coral fungi, and other forms. This study used maximum likelihood methods to determine if there are general trends (evolutionary tendencies) in the evolution of fruiting body forms in homobasidiomycetes, and to estimate the ancestral forms of the homobasidiomycetes and euagarics clade. Character evolution was modeled using a published 481-species phylogeny under two character-coding regimes: additive binary coding, using DISCRETE, and multistate (five-state) coding, using MULTISTATE. Inferences regarding trends in character evolution made under binary coding were often in conflict with those made under multistate coding, suggesting that the additive binary coding approach cannot serve as a surrogate for multistate methods. MULTISTATE was used to develop a"minimal"model of fruiting body evolution, in which the 20 parameters that specify rates of transformations among character states were grouped into the fewest possible rate categories. The minimal model required only four rate categories, one of which is approaching zero, and suggests the following conclusions regarding trends in evolution of homobasidiomycete fruiting bodies: (1) there is an active trend favoring the evolution of pileate-stipitate forms (those with a cap and stalk); (2) the hypothesis that the evolution of gasteroid forms (those with internal spore production, such as puffballs) is irreversible cannot be rejected; and (3) crustlike resupinate forms are not a particularly labile morphology. The latter finding contradicts the conclusions of a previous study that used binary character coding. Ancestral state reconstructions under binary coding suggest that the ancestor of the homobasidiomycetes was resupinate and the ancestor of the euagarics clade was pileate-stipitate, but ancestral state reconstructions under multistate coding did not resolve the ancestral form of either node. The results of this study illustrate the potential sensitivity of comparative analyses to character state definitions.

Advances in the phylogenesis of Agaricales and its higher ranks and strategies for establishing phylogenetic hypotheses

“…The data show that fruitbody form and hymenophore type did not reflect phylogenetic relationships well. Later research has also confirmed this (Hibbett, 2004). Moncalvo et al (2000) investigated phylogenetic relationships within the order Agaricales with analysis of nuclear large subunit ribosomal DNA sequences.…”

An Investigation of the Phylogeny and Evolutionary Processes of Deliquescent Fruiting Bodies in the Mushroom Family Psathyrellaceae (Agaricales)

“…It is evident, that sequestrization, the process that generate the gasteroid fruiting bodies, operates via the reduction or loss of certain structures, such as the stipe, the hymenium or forcible spore discharge (Hibbett 2004, Thiers 1984, Desjardin 2003, Binder et al 2005, Albee-Scott 2007. Thus, gasteroid forms have often been interpreted as reduced forms, although what reduction or simplification means on the cellular or biochemical level is obscure.…”

“…One of the greatest challenges in fungal evolutionary biology is to explain how today's overwhelming diversity of fruiting body types evolved, and what processes and selective forces gave rise to the considerable morphological variability of fruiting body types of extant fungal species (Hibbett and Binder 2002;Desjardin 2003;Hibbett 2004;Binder et al 2005;Albee-Scott 2007). It has been suggested that many of the morphologies are highly adaptive and have evolved and continue to evolve in response to changes in environmental conditions (Peintner et al 2001;Albee-Scott 2007;Hibbett 2007).…”

“…One of these, the unfolding of species complexity has been examined via modeling fruiting body evolution and identifying trends that have generated the diversity of extant forms. A major challenge posed by this question is that the array of fruiting body forms should be satisfactorily coded as discrete characters, either as binary, or multistate (Hibbett 2004). Multistate characters have a higher potential to adequately accommodate the continuum of biological structures into a discrete coding system, whereas binary characters can more easily be modeled in the comparative analyses (Pagel 1994, Cunningham et al 1999, Felsenstein 2004, Hibbett 2004.…”

“…The increasing availability of elaborate phylogenies for specific groups and sequences for a considerable number of species in the Agaricomycetes allowed the examination and modeling of large-scale macroevolutionary processes along branches of phylogenetic trees, an approach called phylogenetic comparative method. Much of the research on evolutionary processes of fungal fruiting bodies relates to the questions of whether resupinate, that is flat, crust-like morphologies represent a derived or ancestral condition, and how the complexity of fruiting bodies changed during evolution (Hibbett and Binder 2002;Hibbett 2004). To the best of our knowledge, there have been no studies that attempted to identify the morphological or physiological traits that accompany significant changes in fruiting body morphologies, and there have been very few attempts to estimate the age of derived morphologies (Bruns et al 1989).…”