The research on the Funariaceae was/is supported by two grants from the US National Science Foundation:
DEB-1146295 (2012-2015): Rapid radiation and sporophyte evolution in the Funariaceae: inferences from phylogenomics and cross generational cuticle development studies.
DEB 0919284 (2009-2012) (Co-PI : Dr. C. Jones; UCONN): Reduction & reversal in the Funariaceae: phylogenetic perspective on sporophyte complexity and role of the calyptra.
Macroevolutionary trends are widely associated with increases in morphological, anatomical or physiological complexity. Complex characters have also been lost multiple times across the tree of life, consequently erasing the evolutionary signature shared by descendants from a unique common ancestor. The result is that phenetically similar taxa are often artificially grouped together. Such has been the case in mosses, where reduction is hypothesized in many lineages and is particularly prevalent in the Funariaceae. Much of our knowledge of fundamental aspects of moss biology is based on studies of members of this family, a significance that continues today with the recent emergence of Physcomitrella patens as a model organism in plant biology. Nevertheless, P. patens is currently a classic example of a morphologically reduced taxon of uncertain phylogenetic placement. Character reduction in the Funariaceae takes several forms, ranging, for example, from virtual loss of the stalk (seta) that elevates the sporangium to reduction in complexity of the spore dispersing structure, the peristome. The structure of the peristome and mode of dehiscence of the sporangium have long been treated as essential systematic characters — the peristome is analogous to the flower in moss classification — yet at the same time frequent reversals render classifications based solely on morphological traits tenuous. To assess polarity of character transformations and the significance of character-states in the family’s evolutionary history, we propose to construct a phylogenetic hypothesis for the Funariaceae based on 15 loci and a minimum of 60 ingroup taxa. Taxon sampling will approach 90% of the generic diversity and represent a broad spectrum of sporophyte reduction. We will score at least 60 morphological characters and reconstruct ancestral character-states to identify synapomorphies and test whether the loss of complex traits is reversible in the Funariaceae. The sporophyte of all bryophytes remains attached to the maternal plant throughout its short life. Maternal care for the developing sporophyte is a unifying feature of all land plants. Mosses are further characterized by a unique maternal plant-sporophyte interaction, one that involves retention of a hat (i.e. the calyptra) of maternal tissue covering the apex of the developing sporophyte. The calyptra is essential for normal sporophyte ontogeny: precocious removal of the calyptra results in sporophyte abortion. The precise mechanism of this interaction is unknown. In this proposal we describe a novel observation: the outer epidermal cells of the calyptra have a relatively well-developed cuticle in Funaria hygrometrica . We suggest that one role of the calyptra is to provide an essential barrier to water loss from the meristematic regions of the sporophyte that lack a proper cuticle. This suggestion in turn leads to the hypothesis that the evolution of sporophyte complexity is linked to the presence of the calyptral cuticle. We will survey the phylogenetic pattern of cuticle deposition on calyptrae using transmission electron microscopy and test for correlations between calyptra cuticular traits and sporophyte complexity to provide phylogenetic evidence for a potential role of the calyptra in preventing dehydration of the sporophyte.
The unique ancestor to bryophytes (mosses) arose in the Devonian, and their evolutionary history over the next 400 million years resulted in approximately 13,000 extant species. Although often considered sphinxes of the past, recent evidence highlights episodes of rapid and sometimes recent diversification events, which at least in one case correlates with global climatic change. Furthermore, below the seemingly simple morphology, hides a broad genetic diversity, distinct ploidy levels and likely also subtle physiological adaptations in these typically desiccation tolerant organisms. Intensive populations sampling over the geographical and ecological spectrum of bryophytes often reveals a robust partitioning of the genetic diversity, indicative of cryptic speciation. Bryophytes have not only withstood extinction, they are dynamic evolutionary entities, which thrive in virtually all terrestrial ecosystems. The macroevolutionary history of mosses is characterized by increasing architectural complexity in the mode of dehiscence and mechanisms controlling spore dispersal. However, these innovations are lost in some lineages, resulting in ancestral character-states defining highly derived taxa, often obfuscating their phylogenetic affinities. Whether such reverse evolution is irreversible or results in a dead-end remains unexplored. Reduction in sporophytic architecture may be correlated to features of the calyptra, a hood of maternal tissue covering the developing sporophyte throughout its growth and providing essential protection against desiccation, until the emerging sporophyte has developed its own waxy cuticle that seals its body off against water loss. The architecture of the hood varies among species and we predict that the shortening of the hood is correlated with a shortening and simplification of the sporophyte or compensated by an acceleration of cuticle development on the sporophyte. We seek to test these two hypotheses using the Funariaceae as our model. This family comprises about 150 species representing a broad gradient in architectural complexity of their spore producing generation and their associated hood. The morphological spectrum is defined by Funaria with long stalks subtending the arched capsule, shedding a lid and bearing two rings of teeth and covered by a large hood, and Physcomitrella, with sessile capsules disintegrating at maturity, lacking mechanisms to control spore release and barely covered by a tiny hood. We will reconstruct the transformations of morphological characters based on a phylogenomic history of the family drawn from all three genomes for a total of 210,000 bps, and characterize cuticle development on the calyptrae and sporophyte of species with contrasting combinations of calyptra and sporophyte sizes.