How phylogenetic inference can shape our view of heterochrony: examples from thecideide brachiopods

Heterochrony is considered to be an important and ubiquitous mechanism of e volutionary change. Three components are necessary to describe heterochrony : phylogenetic relationships, size and shape change, and timing of developm ental events. Patterns and processes of heterochrony are all too often invo ked before all three components have been investigated. Phylogenetic hypoth eses affect the interpretation of heterochrony in three ways: rooting of a clade, topology of a clade, and character polarity. To study these effects we examined the distribution of shell microstructure, lophophore support st ructures, and body size in four different phylogenetic hypotheses of thecid eide brachiopods (Triassic to Recent), a group of minute, cryptic, benthic marine invertebrates. Thecideides are consistently monophyletic in experiments using terebratulid e, strophomenate, and spire-bearing outgroups together and separately, vary ing ingroup membership, and experimentally withholding certain character co mplexes. Thecideide monophyly is also supported by bootstrap analysis. Hypo theses of heterochrony in thecideide origins and evolution are therefore no t merely artifacts of classification and can be pursued further. Using eith er strophomenate or spire-bearing outgroups, Triassic Thecospira is the mos t primitive thecideide. Trees constructed using terebratulide outgroups are rooted instead at Eudesella, a taxon derived in every other phylogenetic r econstruction, and the Triassic thecideides occupy derived rather than prim itive positions. Our phylogenetic results support the traditional interpretation of the redu ction or loss of the secondary fibrous shell layer as a paedomorphic patter n, whereas the evolution of lophophore support structures suggests a peramo rphic pattern. Reduction in thecideide adult body size is gradual, phylogen etically, and results in an overall paedomorphic pattern. Heterochrony in t hese three character suites may play a role in the subsequent evolution of the clade, but apparently not in the origin of the clade, as is commonly th ought. Heterotopy, rather than-or in addition to-heterochrony, may account for both the origin and evolution of the lophophore support structures and in the reduction and loss of the secondary shell layer. These phylogenetic hypotheses suggest that heterochrony can result from a complex mosaic of pr ocesses and provide specific, testable predictions about the processes resp onsible for producing the patterns, whether heterochronic or not. Categoriz ing an entire clade (such as thecideides), rather than individual character s, as globally paedomorphic may allow interesting peramorphic patterns in i ndividual characters to be overlooked.