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

Abstract

Heterochrony is considered to be an important and ubiquitous mechanism of evolutionary change. Three components are necessary to describe heterochrony: phylogenetic relationships, size and shape change, and timing of developmental events. Patterns and processes of heterochrony are all too often invoked before all three components have been investigated. Phylogenetic hypotheses 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 structures, and body size in four different phylogenetic hypotheses of thecideide brachiopods (Triassic to Recent), a group of minute, cryptic, benthic marine invertebrates.Thecideides are consistently monophyletic in experiments using terebratulide, strophomenate, and spire-bearing outgroups together and separately, varying ingroup membership, and experimentally withholding certain character complexes. Thecideide monophyly is also supported by bootstrap analysis. Hypotheses of heterochrony in thecideide origins and evolution are therefore not merely artifacts of classification and can be pursued further. Using either strophomenate or spire-bearing outgroups, Triassic Thecospira is the most primitive thecideide. Trees constructed using terebratulide outgroups are rooted instead at Eudesella, a taxon derived in every other phylogenetic reconstruction, and the Triassic thecideides occupy derived rather than primitive positions.Our phylogenetic results support the traditional interpretation of the reduction or loss of the secondary fibrous shell layer as a paedomorphic pattern, whereas the evolution of lophophore support structures suggests a peramorphic pattern. Reduction in thecideide adult body size is gradual, phylogenetically, and results in an overall paedomorphic pattern. Heterochrony in these 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 thought. 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 processes and provide specific, testable predictions about the processes responsible for producing the patterns, whether heterochronic or not. Categorizing an entire clade (such as thecideides), rather than individual characters, as globally paedomorphic may allow interesting peramorphic patterns in individual characters to be overlooked.

<p class="HeadingRunIn"><strong>Discovery of Recent thecideide brachiopods (Order: Thecideida, Family: Thecideidae) in Sulawesi, Indonesian Archipelago, with implications for reproduction and shell size in the genus <em>Ospreyella</em></strong></p>

“…This observation implies that shell size influences the development of the brachidium. Actually, heterochrony is known to be a common phenomenon in thecideide evolution (Jaecks & Carlson 2001). However, it remains to be seen whether the shell size can be triggered by environmental factors or is genetically fixed within a lineage.…”

The Evolution of Brachiopoda

“…The relationship between evolution and development has long been a focus of attention among brachiopod workers, from Beecher (1891) to Atkins (1959) to Jaecks & Carlson (2001). The evolutionary consequences of changes in developmental rate and timing, referred to as heterochrony (Haeckel 1875, Alberch et al 1979, can result in paedomorphic or peramorphic patterns of evolutionary change.…”

“…The evolutionary consequences of changes in developmental rate and timing, referred to as heterochrony (Haeckel 1875, Alberch et al 1979, can result in paedomorphic or peramorphic patterns of evolutionary change. Because of their relatively simple external shape and relatively large adult body size, terebratulide brachiopods have been claimed to be neotenic (A. Williams, personal communication); tiny thecideides may be progenetic ( Jaecks & Carlson 2001). Very small adult body size, observed in all thecideide and a number of extant terebratulide and rhynchonellide brachiopod species (Motchurova-Dekova et al 2002), determines many aspects of life history: Brooders are often small as adults and produce fewer gametes over their life span than do free-spawners; small adults may have shorter life spans, or grow at slower rates, and reach sexual maturity earlier than large adults; small adults interact with their ambient fluid environment differently than do large adults.…”

“…The complex brachial ridges that support the thecideide lophophore strongly suggest a peramorphic, not paedomorphic, pattern as well. Rather than characterizing entire clades as paedomorphic or peramorphic, it is more informative to focus on suites of individual characters and the mosaic of heterochronic patterns they exhibit ( Jaecks & Carlson 2001).…”

Anchors and snorkels: heterochrony, development and form in functionally constrained fossil crassatellid bivalves

“…Investigations of heterochrony require size, shape, and ontogenetic age data, and a phylogenetic framework within which ancestor-descendant relationships can be identified (Jaecks and Carlson 2001). However, age data can be problematic to gather, particularly for extinct species (Jones and Gould 1999).…”