Pollination syndromes and the origins of floral traits.

BACKGROUND: A general view in the study of pollination syndromes is that floral traits usually represent convergent floral adaptations to specific functional pollinator groups. However, the definition of convergence is elusive and contradictory in the literature. Is convergence the independent evolution of either the same trait or similar traits with the same function? A review of the concept of convergence in developmental biology and phylogenetic systematics may shed new light in studies of pollination syndromes. SCOPE: The aims of this article are (1) to explore the notion of convergence and other concepts (analogy, homoplasy and parallelism) within the theory and practice of developmental evolution and phylogenetic systematics; (2) to modify the definitions of syndromes in order to embrace the concepts of analogy and convergence; (3) to revisit the bat pollination syndrome in the context of angiosperm phylogeny, with focus on the showy 'petaloid' organs associated with the syndrome; (4) to revisit the genetic-developmental basis of flower colour; (5) to raise evolutionary hypotheses of floral evolution associated with the bat pollination syndrome; and (6) to highlight some of the current frontiers of research on the origin and evolution of flowers and its impact on pollination syndrome studies in the 21st century. CONCLUSIONS: The inclusion of the concepts of analogy and convergence within the concept of syndromes will constitute a new agenda of inquiry that integrates floral biology, phylogenetic systematics and developmental biology. Phyllostomid and pteropodid bat pollination syndrome traits in eudicots and monocots represent cases of analogous and convergent evolution. Pollination syndromes are a multivariate concept intrinsically related to the understanding of flower organogenesis and evolution. The formulation of hypotheses of pollination syndromes must consider the phylogenetic levels of universality for both plant and animal taxa, flower development, genetics, homology and evolution, and a clear definition of evolutionary concepts, including analogy, convergence, homoplasy and parallelism.

A unified view of homology.

As it spread through time and into distinct areas of science-from comparative anatomy to evolutionary biology, cladistics, developmental and molecular biology-the homology concept has changed considerably, presenting various meanings. Despite many attempts at developing a comprehensive understanding of the concept, this context-sensitive notion of homology has been a subject of an ongoing debate. Inspired by that and following Kevin de Queiroz and Richard Mayden's view on species concept and delimitation, we presented in this article an attempt to systematize and advance the understanding of the homology problem. Our main goals were: (i) to present a comprehensive checklist of 'concepts of homology'; (ii) to identify which are really concepts with ontological definitions (theoretically rooted in structural correspondence and common ancestry), and which are, in fact, not concepts, but epistemological (empirical and methodological) criteria of homology delimitation; (iii) to provide a synonymy of the concepts and criteria of homology delimitation; (iv) to present a hierarchy of homology concepts within Hennig's hologenetic system; and (v) to endorse the adoption of a unified view of homology by treating homology as a correspondence of spatio-temporal properties (genetic, epigenetic, developmental and positional) at the level of the individual, species or monophyletic group. We found 59 'concepts of homology' in the literature, from which 34 were categorically treated as concepts, 17 as criteria of homology delimitation, Four were excluded from our treatment, and Müller's five concepts were rather treated as approaches to homology. Homology concepts and criteria were synonymized based on structural correspondence, replicability, common ancestry, genetic and epigenetic developmental causes, position and optimization. Regarding the synonymy, we conclusively recognized 21 different concepts of homology, and five empirical and four methodological criteria. Hierarchical ontological aspects of homology were systematized under Hennig's hologenetic system, based on the existence of ontogenetic, tokogenetic and phylogenetic levels of homology. The delimitation of tokogenetic and phylogenetic homologies depends on optimization criteria. The unified view of homology is discussed in the context of the ancestral angiosperm flower.

The semaphorontic view of homology.

The relation of homology is generally characterized as an identity relation, or alternatively as a correspondence relation, both of which are transitive. We use the example of the ontogenetic development and evolutionary origin of the gnathostome jaw to discuss identity and transitivity of the homology relation under the transformationist and emergentist paradigms respectively. Token identity and consequent transitivity of homology relations are shown to be requirements that are too strong to allow the origin of genuine evolutionary novelties. We consequently introduce the concept of compositional identity that is grounded in relations prevailing between parts (organs and organ systems) of a whole (organism). We recognize an ontogenetic identity of parts within a whole throughout the sequence of successive developmental stages of those parts: this is an intra-organismal character identity maintained throughout developmental trajectory. Correspondingly, we recognize a phylogenetic identity of homologous parts within two or more organisms of different species: this is an inter-species character identity maintained throughout evolutionary trajectory. These different dimensions of character identity--ontogenetic (through development) and phylogenetic (via shared evolutionary history)--break the transitivity of homology relations. Under the transformationist paradigm, the relation of homology reigns over the entire character (-state) transformation series, and thus encompasses the plesiomorphic as well as the apomorphic condition of form. In contrast, genuine evolutionary novelties originate not through transformation of ancestral characters (-states), but instead through deviating developmental trajectories that result in alternate characters. Under the emergentist paradigm, homology is thus synonymous with synapomorphy.

Homology assessment in parsimony and model-based analyses: two sides of the same coin.

The present paper is mainly concerned with homology assessment through phylogenetic analyses. It raises a fundamental question: What are the epistemological differences between modern parsimony and model-based analyses in relation to homology assessment and phylogenetic inference? Although these methods usually achieve concordant topological results, they may generate discordant inferences of character evolution from the same datasets. This indicates that method selection has serious implications for evolutionary scenarios and classificatory arrangements. Notwithstanding that parsimony and model-based approaches use the Hennigian concepts of monophyly and synapomorphy, they employ different epistemological ways of dealing with the monophyly/synapomorphy relationship. Independently of their differences, these analyses should take into account all relevant evidence in support of the phylogenetic inferences. A focus on morphological homologues means that they must be included in data matrices, evaluated as part of the phylogenetic analysis, and cannot be ignored in calculation of the tree(s) length (parsimony), maximum-likelihood (maximum-likelihood), and posterior probabilities (Bayes).

Does counting species count as taxonomy? On misrepresenting systematics, yet again.

Recent commentary by Costello and collaborators on the current state of the global taxonomic enterprise attempts to demonstrate that taxonomy is not in decline as feared by taxonomists, but rather is increasing by virtue of the rate at which new species are formally named. Having supported their views with data that clearly indicate as much, Costello et al. make recommendations to increase the rate of new species descriptions even more. However, their views appear to rely on the perception of species as static and numerically if not historically equivalent entities whose value lie in their roles as "metrics". As such, their one-dimensional portrayal of the discipline, as concerned solely with the creation of new species names, fails to take into account both the conceptual and epistemological foundations of systematics. We refute the end-user view that taxonomy is on the rise simply because more new species are being described compared with earlier decades, and that, by implication, taxonomic practice is a formality whose pace can be streamlined without considerable resources, intellectual or otherwise. Rather, we defend the opposite viewpoint that professional taxonomy is in decline relative to the immediacy of the extinction crisis, and that this decline threatens not just the empirical science of phylogenetic systematics, but also the foundations of comparative biology on which other fields rely. The allocation of space in top-ranked journals to propagate views such as those of Costello et al. lends superficial credence to the unsupportive mindset of many of those in charge of the institutional fate of taxonomy. We emphasize that taxonomy and the description of new species are dependent upon, and only make sense in light of, empirically based classifications that reflect evolutionary history; homology assessments are at the centre of these endeavours, such that the biological sciences cannot afford to have professional taxonomists sacrifice the comparative and historical depth of their hypotheses in order to accelerate new species descriptions.

Are monophyly and synapomorphy the same or different? Revisiting the role of morphology in phylogenetics.

Species are groups of organisms, marked out by reproductive (replicative) properties. Monophyletic taxa are groups of species, marked out by synapomorphies. In Nelson's analysis, monophyly and synapomorphy are identical relations. Monophyly and synapomorphy, however, are not equivalent relations. Monophyly is epistemically not accessible, whereas synapomorphy is epistemically accessible through character analysis. Monophyly originates with speciation, the two sister-species that come into being through the splitting of the ancestral species lineage forming a monophyletic taxon at the lowest level of inclusiveness. Synapomorphy provides the empirical evidence for monophyly, inferred from character analysis in the context of a three-taxon statement. If synapomorphy and monophyly were equivalent, phylogenetic systematists should find a single tree, instead of multiple equally parsimonious trees. Understanding synapomorphy as the relevant evidence for phylogenetic inference reveals a category mistake in contemporary phylogenetics: the treatment of morphological characters mapped onto molecular trees as synapomorphies and homoplasies. The mapping of morphological characters onto nodes of a molecular tree results in an empirically empty procedure for synapomorphy discovery. Morphological synapomorphies and homoplasies can only be discovered by morphological and combined analyses. The use of morphology in phylogenetic inference in general is defended by examples from Laurales and Squamata in particular. To make empirical evidence scientifically relevant in order to search for concordance, or dis-concordance, of phylogenetic signal, is certainly more fruitful for phylogenetics than the uncritical mapping of morphological traits on a molecular scaffold. © The Willi Hennig Society 2010.

Coherence, correspondence, and the renaissance of morphology in phylogenetic systematics.

The decline in morphological phylogenies has become a pronounced trend in contemporary systematics due to a disregard for theoretical, methodological, conceptual, and philosophical approaches. The role and meaning of morphology in phylogenetic reconstruction and classification have been undermined by the following: (i) the ambiguous delineation of morphological characters; (ii) the putative "objectivity" of molecular data; (iii) that morphology has not been included in data matrices; (iv) that morphology has been mapped onto molecular cladograms; and (v) a separation of a paradigmatic relationship among morphology, phylogeny, and classification. Historical/philosophical arguments including the synthesis of coherence (coherentism) and correspondence (foundationalism) theories-i.e. "foundherentism" as a theory of epistemic justification-provide support for a renaissance of morphology in phylogenetic systematics. In the language of systematics, coherence theory corresponds to the logical/operational congruence of character states translated into a hierarchical/relational system of homologues and monophyletic groups as natural kinds. Correspondence theory corresponds to the empirical/causal accommodation of homologues and monophyletic groups as natural kinds grounded in the concept of semaphoront, and in developmental biology, genetics, inheritance, ontogenesis, topology, and connectivity. The role and meaning of morphology are also discussed in the context of separate and combined analyses, palaeontology, natural kinds, character concepts, semaphoront, modularity, and taxonomy. Molecular systematics suffers from tension between coherence and correspondence theories, and fails to provide a pragmatic language for predicates in science and in everyday life. Finally, the renaissance of morphology is not only dependent on a scientific/philosophical perspective but also depends on political, economic, social, and educational reforms in contemporary systematics. © The Willi Hennig Society 2009.

Unbuttoning the Ancestral Flower of Angiosperms.

A recent study using an extensive data set plus sophisticated analytical tools reconstructed a model of the ancestral angiosperm flower. Although attractive, it presents problems of homology assessment. We discuss its inconsistencies and endorse the use of a comparative model that integrates biological parameters as essential to elucidate floral evolution.