Sylvain Gerber

A superarmored lobopodian from the Cambrian of China and early disparity in the evolution of Onychophora

Significance Paleozoic lobopodians constitute a diverse assemblage of worm-like organisms that are known from various exceptional fossil deposits and were among the earliest animals to develop skeletonized body parts for protection. Here, we describe Collinsium ciliosum gen. et sp. nov., an armored lobopodian from the early Cambrian Xiaoshiba Lagerstätte (South China). Collinsium belongs to an extinct clade of superarmored lobopodians characterized by supernumerary dorsal spines, and specialized limbs for filter feeding; collectively, these fossil taxa represent a well-defined group within the lineage leading to extant velvet worms (Onychophora). Despite their greater morphological variety and appendage complexity compared with other lobopodians and extant velvet worms, Collinsium and its close relatives embodied a unique, yet ultimately failed, autoecology during the Cambrian explosion. We describe Collinsium ciliosum from the early Cambrian Xiaoshiba Lagerstätte in South China, an armored lobopodian with a remarkable degree of limb differentiation including a pair of antenna-like appendages, six pairs of elongate setiferous limbs for suspension feeding, and nine pairs of clawed annulated legs with an anchoring function. Collinsium belongs to a highly derived clade of lobopodians within stem group Onychophora, distinguished by a substantial dorsal armature of supernumerary and biomineralized spines (Family Luolishaniidae). As demonstrated here, luolishaniids display the highest degree of limb specialization among Paleozoic lobopodians, constitute more than one-third of the overall morphological disparity of stem group Onychophora, and are substantially more disparate than crown group representatives. Despite having higher disparity and appendage complexity than other lobopodians and extant velvet worms, the specialized mode of life embodied by luolishaniids became extinct during the Early Paleozoic. Collinsium and other superarmored lobopodians exploited a unique paleoecological niche during the Cambrian explosion.

What limits the morphological disparity of clades

The morphological disparity of species within major clades shows a variety of trajectory patterns through evolutionary time. However, there is a significant tendency for groups to reach their maximum disparity relatively early in their histories, even while their species richness or diversity is comparatively low. This pattern of early high-disparity suggests that there are internal constraints (e.g. developmental pleiotropy) or external restrictions (e.g. ecological competition) upon the variety of morphologies that can subsequently evolve. It has also been demonstrated that the rate of evolution of new character states decreases in most clades through time (character saturation), as does the rate of origination of novel bodyplans and higher taxa. Here, we tested whether there was a simple relationship between the level or rate of character state exhaustion and the shape of a clades disparity profile: specifically, its centre of gravity (CG). In a sample of 93 extinct major clades, most showed some degree of exhaustion, but all continued to evolve new states up until their extinction. Projection of states/steps curves suggested that clades realized an average of 60% of their inferred maximum numbers of states. Despite a weak but significant correlation between overall levels of homoplasy and the CG of clade disparity profiles, there were no significant relationships between any of our indices of exhaustion curve shape and the clade disparity CG. Clades showing early high-disparity were no more likely to have early character saturation than those with maximum disparity late in their evolution.

Not all roads can be taken: development induces anisotropic accessibility in morphospace.

Morphospaces are quantitative representations of phenotype space that are widely used in studies of morphological evolution. Do current conceptualizations of morphospaces, however, appropriately reflect the evolutionary dynamics of organisms depicted in these spaces? Most empirical morphospace studies implicitly consider variability of biological forms as isotropic, but such a view appears inadequate when the properties of development mediating phenotypic changes are considered. Here, a trilobite case study is used to visualize the constraints imposed by development on the accessibility structure of morphospace. Variability in the resultant morphospace is strongly anisotropic and reveals discordances between the apparent range of possible phenotypes and their actual accessibility. Homoplasy, directionality, and asymmetry of evolutionary transitions appear as natural consequences of anisotropic variability and point out the limitation of morphological distance for evolutionary inference. Measures of distance in morphospace should be used with considerable caution and must be complemented with developmentally meaningful measures of evolutionary accessibility.

How (much) do flowers vary? Unbalanced disparity among flower functional modules and a mosaic pattern of morphospace occupation in the order Ericales

The staggering diversity of angiosperms and their flowers has fascinated scientists for centuries. However, the quantitative distribution of floral morphological diversity (disparity) among lineages and the relative contribution of functional modules (perianth, androecium and gynoecium) to total floral disparity have rarely been addressed. Focusing on a major angiosperm order (Ericales), we compiled a dataset of 37 floral traits scored for 381 extant species and nine fossils. We conducted morphospace analyses to explore phylogenetic, temporal and functional patterns of disparity. We found that the floral morphospace is organized as a continuous cloud in which most clades occupy distinct regions in a mosaic pattern, that disparity increases with clade size rather than age, and that fossils fall in a narrow portion of the space. Surprisingly, our study also revealed that among functional modules, it is the androecium that contributes most to total floral disparity in Ericales. We discuss our findings in the light of clade history, selective regimes as well as developmental and functional constraints acting on the evolution of the flower and thereby demonstrate that quantitative analyses such as the ones used here are a powerful tool to gain novel insights into the evolution and diversity of flowers.

Modularity and developmental stability in segmented animals: variation in translational asymmetry in geophilomorph centipedes

Does a modular body organization present a challenge for developmental control? We investigate the idea of a possible developmental cost of modularity by examining the relationship between modularity and developmental stability in a multi-segmented arthropod taxon: the geophilomorph centipedes. In a sample of eight species, we tested the correlation between developmental stability, estimated from measures of translational fluctuating asymmetry, and the number of trunk segments and some other morphological traits, both at the species and individual levels. We found sizeable differences in size and shape patterns of variation at the level of species. However, we did not find any clear evidence of correlation between fluctuating asymmetry and the number of trunk segments or the other morphological traits considered. Thus, our results provide no support to the idea of a possible trade-off between the cardinality of a modular system and the level of developmental precision in the phenotypic expression of its modules. The results of this exploratory study invite further investigations of patterns of translational fluctuating asymmetry in segmented animals and other modular organisms, as these have the potential to reveal features of developmental stability that cannot be captured by the study of bilateral asymmetry alone.

The geometry of morphospaces: lessons from the classic Raup shell coiling model

Morphospaces are spatial depictions of morphological variation among biological forms that have become an integral part of the analytical toolkit of evolutionary biologists and palaeobiologists. Nevertheless, the term morphospace brings together a great variety of spaces with different geometries. In particular, many morphospaces lack the metric properties underlying the notions of distance and direction, which are, however, central to the analysis of morphological differences and evolutionary transitions. The problem is illustrated here with the iconic morphospace of coiled shells implemented by Raup 50 years ago. The model, which allows the description of shell coiling geometry of various invertebrate taxa, is a seminal reference in theoretical morphology and morphospace theory, but also a morphometric framework frequently used in empirical studies, particularly of ammonoids. Because of the definition of its underlying parameters, Raups morphospace does not possess a Euclidean structure and a meaningful interpretation of the spread and spacing of taxa within it is not guaranteed. Focusing on the region of the morphospace occupied by most ammonoids, I detail a landmark‐based morphospace circumventing this problem and built from the same input measurements required for the calculation of Raups parameters. From simulations and a reanalysis of Palaeozoic ammonoid shell disparity, the properties of these morphospaces are compared and their algebraic and geometric relationships highlighted. While Raups model remains a valuable tool for describing ammonoid shells and relating their shapes to the coiling process, it is demonstrated that quantitative analyses of morphological patterns should be carried out within the landmark‐based framework. Beyond this specific case, the increasing use and diversity of morphospaces in evolutionary morphology call for caution when interpreting patterns and comparing results drawn from different types of morphospaces.

Hunting Darwin's Snark: which maps shall we use?

The 11 contributions to this thematic volume touch on a large range of issues concerning the landscape of biological possibilities and the manner by which it may be traversed by evolving life forms. The contributors also consider how this landscape might be mapped by evolutionary biologists, with an emphasis on how one might identify the limits of such maps. While some agreements emerge on the question of limits on evolution, not surprisingly few contributors look towards the same horizons. Rather than providing a potted summary of the 11 papers, our aim in this introduction is to identify eight principal themes that might serve as common ground and, as importantly, to listen out for the sound of rushing subterranean waters that hint at caverns of concealed knowledge. By no means all of these themes are addressed by all authors, but in gathering the many strands of enquiry we hope that this will allow us to ask: What, if any, are the limits to evolution?