Modular marvels: The ecology, evolvability, and energetics of bryozoan polymorphism

<p>Modularity is a fundamental concept in biology. Most taxa within the colonial invertebrate phylum Bryozoa have achieved division of labor through the development of specialized modules (polymorphs), and this group is perhaps the most outstanding exemplar of the phenomenon. This thesis addresses several gaps in the literature concerning the morphology, ecology, energetics, and evolvability of bryozoan polymorphism. It has been over 40 years since the last review of bryozoan polymorphism, and here I provide a comprehensive update that describes the diversity, morphology, and function of bryozoan polymorphs and the significance of modularity to their evolutionary success. While the degree of module compartmentalization is important for the evolution of polymorphism in bryozoans, this does not appear to be the case for other colonial invertebrates. To facilitate data collection, I developed a classification system for polymorphism in cheilostome bryozoans. While classification systems exist for bryozoan colony form, the system presented here is the first developed for polymorphism. This system is fully illustrated and non-hierarchical, enabling swift classification and statistical comparisons at many levels of detail. Understanding community assembly is a key goal in community ecology, but previous work on bryozoan communities has focused on colony form rather than polymorphism. Environmental filtering influences community assembly by excluding ill-adapted species, resulting in communities with similar functional traits. An RLQ (a four-way ordination) analysis incorporating spatial data was run on a dataset of 642 species of cheilostomes from 779 New Zealand sites, to investigate environmental filtering of colony form and zooid polymorphism. This revealed environmental filtering of colony form: encrusting-cemented taxa were predominant in shallow environments with hard substrata (200 m). Furthermore, erect taxa found in shallow environments with high current speeds were typically jointed. Surprisingly, polymorphism also followed environmental gradients. External ovicells (brood chambers) were more common in deeper, low oxygen water than immersed and internal ovicells. This may reflect the oxygen needs of the embryo or increased predation intensity in shallow environments. Bryozoans with costae (rib-like spines) tended to be found in deeper water as well, while bryozoans with calcified frontal shields were found in shallow environments with a higher concentration of CaCO₃. Avicularia (defensive grasping structures) were not related to environmental conditions, and changes in pivot bar structure with depth likely represent a phylogenetic signal. Factors influencing community assembly were somewhat partitioned by levels of organization, since colony form responds to environmental conditions, while the effects of evolutionary history, predation, and environmental conditions were not well-separated for zooid-level morphology. Finally, rootlets may have been a key innovation that allowed cementing taxa to escape hard substrata, potentially contributing to the cheilostome radiation. Despite the diversity of life on earth, many morphologies have not been achieved. Morphology can be limited by a variety of constraints (developmental, historical, biomechanical) and comparing the distribution of realized forms in a theoretical form-space (i.e. “morphospace”) can highlight which constraints are at play and potential functions. If traits cluster around biomechanical optima, then morphology may be shaped by strong selective pressures. In contrast, a well-explored (filled) morphospace suggests weak constraints and high morphological evolvability. Here, constraints on morphospace exploration were examined for 125 cheilostome bryozoan species from New Zealand. The mandible morphospaces for avicularia (beak-like polymorphs) were visualized using Coordinate-Point Extended Eigenshape analysis. Mechanical advantage, moment of inertia, drag, peak force, and rotational work required to close the mandible were calculated for theoretical (n=47) and real mandibles (n=224) to identify biomechanical optima. The volume and surface of area of the parcel of water passed through by the closing mandible (referred to as the “domain”) was also calculated. The theoretical morphospace of avicularia is well-explored, suggesting they are highly evolvable and have relaxed developmental constraints. However, there may be constraints within lineages. A well-developed fulcrum (complete pivot bar) may be an evolutionary pre/corequisite to evolving mandibles with extreme moments of inertia such as setose and highly spathulate forms. The most common mandible shape, triangular, represents a trade-off between maximizing domain size, minimizing energetic cost (force and construction material), and minimizing the potential for breakage. This suggests that they are well suited for catching epibionts, representing the first empirical evidence for avicularian function. Tendon length and mechanical advantage are limited by tendon width, which itself is constrained by the base width of the mandible. This explains the low mechanical advantage of setose mandibles and suggests that they are unable to grasp epibionts. The calories required to close the mandible of an avicularium (estimated from rotational work) are quite small (1.24 x 10⁻¹⁶ to 8.82 x 10⁻¹¹ cal). Overall, this thesis highlights the complexity of bryozoan polymorphism and suggests cheilostome avicularia could provide a unique evolutionary system to study due to their apparent lack of strong developmental constraints. Future studies into the ecology of polymorphism should focus on the degree of investment (polymorph abundance within a colony) rather than presence or absence.</p>

Modular marvels: The ecology, evolvability, and energetics of bryozoan polymorphism

<p>Modularity is a fundamental concept in biology. Most taxa within the colonial invertebrate phylum Bryozoa have achieved division of labor through the development of specialized modules (polymorphs), and this group is perhaps the most outstanding exemplar of the phenomenon. This thesis addresses several gaps in the literature concerning the morphology, ecology, energetics, and evolvability of bryozoan polymorphism. It has been over 40 years since the last review of bryozoan polymorphism, and here I provide a comprehensive update that describes the diversity, morphology, and function of bryozoan polymorphs and the significance of modularity to their evolutionary success. While the degree of module compartmentalization is important for the evolution of polymorphism in bryozoans, this does not appear to be the case for other colonial invertebrates. To facilitate data collection, I developed a classification system for polymorphism in cheilostome bryozoans. While classification systems exist for bryozoan colony form, the system presented here is the first developed for polymorphism. This system is fully illustrated and non-hierarchical, enabling swift classification and statistical comparisons at many levels of detail. Understanding community assembly is a key goal in community ecology, but previous work on bryozoan communities has focused on colony form rather than polymorphism. Environmental filtering influences community assembly by excluding ill-adapted species, resulting in communities with similar functional traits. An RLQ (a four-way ordination) analysis incorporating spatial data was run on a dataset of 642 species of cheilostomes from 779 New Zealand sites, to investigate environmental filtering of colony form and zooid polymorphism. This revealed environmental filtering of colony form: encrusting-cemented taxa were predominant in shallow environments with hard substrata (200 m). Furthermore, erect taxa found in shallow environments with high current speeds were typically jointed. Surprisingly, polymorphism also followed environmental gradients. External ovicells (brood chambers) were more common in deeper, low oxygen water than immersed and internal ovicells. This may reflect the oxygen needs of the embryo or increased predation intensity in shallow environments. Bryozoans with costae (rib-like spines) tended to be found in deeper water as well, while bryozoans with calcified frontal shields were found in shallow environments with a higher concentration of CaCO₃. Avicularia (defensive grasping structures) were not related to environmental conditions, and changes in pivot bar structure with depth likely represent a phylogenetic signal. Factors influencing community assembly were somewhat partitioned by levels of organization, since colony form responds to environmental conditions, while the effects of evolutionary history, predation, and environmental conditions were not well-separated for zooid-level morphology. Finally, rootlets may have been a key innovation that allowed cementing taxa to escape hard substrata, potentially contributing to the cheilostome radiation. Despite the diversity of life on earth, many morphologies have not been achieved. Morphology can be limited by a variety of constraints (developmental, historical, biomechanical) and comparing the distribution of realized forms in a theoretical form-space (i.e. “morphospace”) can highlight which constraints are at play and potential functions. If traits cluster around biomechanical optima, then morphology may be shaped by strong selective pressures. In contrast, a well-explored (filled) morphospace suggests weak constraints and high morphological evolvability. Here, constraints on morphospace exploration were examined for 125 cheilostome bryozoan species from New Zealand. The mandible morphospaces for avicularia (beak-like polymorphs) were visualized using Coordinate-Point Extended Eigenshape analysis. Mechanical advantage, moment of inertia, drag, peak force, and rotational work required to close the mandible were calculated for theoretical (n=47) and real mandibles (n=224) to identify biomechanical optima. The volume and surface of area of the parcel of water passed through by the closing mandible (referred to as the “domain”) was also calculated. The theoretical morphospace of avicularia is well-explored, suggesting they are highly evolvable and have relaxed developmental constraints. However, there may be constraints within lineages. A well-developed fulcrum (complete pivot bar) may be an evolutionary pre/corequisite to evolving mandibles with extreme moments of inertia such as setose and highly spathulate forms. The most common mandible shape, triangular, represents a trade-off between maximizing domain size, minimizing energetic cost (force and construction material), and minimizing the potential for breakage. This suggests that they are well suited for catching epibionts, representing the first empirical evidence for avicularian function. Tendon length and mechanical advantage are limited by tendon width, which itself is constrained by the base width of the mandible. This explains the low mechanical advantage of setose mandibles and suggests that they are unable to grasp epibionts. The calories required to close the mandible of an avicularium (estimated from rotational work) are quite small (1.24 x 10⁻¹⁶ to 8.82 x 10⁻¹¹ cal). Overall, this thesis highlights the complexity of bryozoan polymorphism and suggests cheilostome avicularia could provide a unique evolutionary system to study due to their apparent lack of strong developmental constraints. Future studies into the ecology of polymorphism should focus on the degree of investment (polymorph abundance within a colony) rather than presence or absence.</p>

Mammalian face as an evolutionary novelty

The anterior end of the mammalian face is characteristically composed of a semimotile nose, not the upper jaw as in other tetrapods. Thus, the therian nose is covered ventrolaterally by the “premaxilla,” and the osteocranium possesses only a single nasal aperture because of the absence of medial bony elements. This stands in contrast to those in other tetrapods in whom the premaxilla covers the rostral terminus of the snout, providing a key to understanding the evolution of the mammalian face. Here, we show that the premaxilla in therian mammals (placentals and marsupials) is not entirely homologous to those in other amniotes; the therian premaxilla is a composite of the septomaxilla and the palatine remnant of the premaxilla of nontherian amniotes (including monotremes). By comparing topographical relationships of craniofacial primordia and nerve supplies in various tetrapod embryos, we found that the therian premaxilla is predominantly of the maxillary prominence origin and associated with mandibular arch. The rostral-most part of the upper jaw in nonmammalian tetrapods corresponds to the motile nose in therian mammals. During development, experimental inhibition of primordial growth demonstrated that the entire mammalian upper jaw mostly originates from the maxillary prominence, unlike other amniotes. Consistently, cell lineage tracing in transgenic mice revealed a mammalian-specific rostral growth of the maxillary prominence. We conclude that the mammalian-specific face, the muzzle, is an evolutionary novelty obtained by overriding ancestral developmental constraints to establish a novel topographical framework in craniofacial mesenchyme.

How development affects evolution

How development affects evolution. A mathematical framework that explicitly integrates development into evolution has recently been derived. Here we use this framework to analyse how development affects evolution. We show that, whilst selection pushes genetic and phenotypic evolution uphill on the fitness landscape, development determines the admissible evolutionary pathway, such that evolutionary outcomes occur at path peaks, which need not be peaks of the fitness landscape. Development can generate path peaks, triggering adaptive radiations, even on constant, single-peak landscapes. Phenotypic plasticity, niche construction, extra-genetic inheritance, and developmental bias variously alter the evolutionary path and hence the outcome. Selective development, whereby phenotype construction may point in the adaptive direction, may induce evolution either towards or away landscape peaks depending on the developmental constraints. Additionally, developmental propagation of phenotypic effects over age allows for the evolution of negative senescence. These results help explain empirical observations including punctuated equilibria, the paradox of stasis, the rarity of stabilizing selection, and negative senescence, and show that development has a major role in evolution.

Developmental integration cannot explain major features of stomatal anatomical evolution in seed plants

Developmental integration can cause traits to covary over macroevolutionary time and in some cases prevent populations from reaching their adaptive optima. Developmental integration between stomatal size and density may contribute to two major features of stomatal anatomical evolution: inverse size-density scaling and bimodal stomatal ratio. If these patterns result from developmental integration, we predicted that in amphistomatous leaves 1) stomatal size and density should covary similarly on both abaxial and adaxial surfaces and 2) stomatal traits (size and density) on each surface should covary isometrically. We synthesized data on stomatal density and length from amphistomatous leaves of 711 terrestrial seed plant taxa mostly from the literature. We estimated the covariance in divergence between stomatal traits from 327 phylogenetically independent contrasts using a robust Bayesian model. Adaxial stomatal density, but not length, is evolutionarily labile and not strongly integrated with stomatal length or abaxial stomatal density. Hence, developmental integration alone cannot explain inverse size-density scaling nor bimodal stomatal ratio. Quasi-independent evolution of stomatal anatomical traits facilitates largely unfettered access to fitness optima. If stomatal anatomical traits are near their current fitness optimum, this implies that limits on trait (co)variance result from selective rather than developmental constraints. However, we cannot rule out that developmental integration is important in some lineages. Future research should identify the mechanistic basis of(dis)integration in stomatal development.

An early burst in brachiopod evolution corresponding with significant climatic shifts during the Great Ordovician Biodiversification Event

We employ modified tip-dating methods to date divergence times within the Strophomenoidea, one of the most abundant and species-rich brachiopod clades to radiate during the Great Ordovician Biodiversification Event (GOBE), to determine if significant environmental changes at this time correlate with the diversification of the clade. Models using origination, extinction and sampling rates to estimate prior probabilities of divergence times strongly support both high rates of anatomical change per million years and rapid divergences shortly before the clade first appears in the fossil record. These divergence times indicate much higher rates of cladogenesis than are typical of brachiopods during this interval. The correspondence of high speciation rates and high anatomical disparity suggests punctuated (speciational) change drove the high frequencies of early anatomical change, which in turn suggests increased ecological opportunities rather than shifting developmental constraints account for high rates of anatomical change. The pulse of rapid evolution began coincident with cooling temperatures, the start of major oscillations in sea level and increased levels of atmospheric oxygen. Our results suggest that these factors permitted major geographical and ecological expansion of strophomenoids with intervals of geographical isolation, resulting in elevated speciation rates and corresponding elevated frequencies of punctuated change.

Evolutionary origins of sexual dimorphism : Lessons from female-limited mimicry in butterflies.

The surprising female-limited mimicry observed in some species is a text-book example of sexually-dimorphic trait submitted to intense natural selection. Two main hypotheses have been proposed to explain female-limited mimicry in butterflies. Predation pressure favouring mimicry could be higher in females because of their slower flight, and overcome developmental constraints favouring the ancestral trait that limits the evolution of mimicry in males but not in females. Alternatively, the evolution of mimicry in males could be limited by sexual selection, generated by females preference for non-mimetic males. However, the evolutionary origin of female preference for non-mimetic males remains unclear. Here, we hypothesise that costly sexual interactions between individuals from distinct sympatric species might intensify because of mimicry, therefore promoting female preference for non-mimetic trait. Using a mathematical model, we compare the evolution of female-limited mimicry when assuming either alternative hypotheses. We show that the patterns of divergence of male and female trait from the ancestral traits can differ between these selection regimes but we specifically highlight that divergence in females trait is not a signature of the effect of natural selection. Altogether, our model reveals the complex interplay between sexual and natural selection shaping the evolution of sexually-dimorphic traits.

The Retrocalcarine Sulcus Is Functionally Distinct Between Macaques and Humans

Primate cerebral cortex is highly convoluted with much of the cortical surface buried in sulcal folds. The origins of cortical folding and its functional relevance has been a major focus of systems and cognitive neuroscience. Stereotyped patterns of cortical folding across individuals and multiple primate species indicate common evolutionary pressures in their development. However, foundational questions regarding organizing principles shared across species remain unanswered. Taking a cross-species comparative approach with a careful consideration of historical observations, we investigate cortical folding within the calcarine sulcus, a primary fold in primates. We identify two macroanatomical structures – the retrocalcarine and external calcarine sulci – in 24 humans and 6 macaque monkeys. We show that within species, these sulci are identifiable in all individuals, fall on a similar part of the V1 retinotopic map, and thus, serve as anatomical landmarks predictive of functional organization. Yet, across species, the actual underlying visual field representations differ strikingly across humans and macaques. Thus, the structure-function correspondence for an evolutionarily old structure like V1 is species-specific and suggests intriguing differences in developmental constraints across primates.