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>

Validity of Mechanical advantage hypothesis of human grasping depends on the nature of task difficulty

Successful object interaction during daily living involves maintaining the grasped object in a static equilibrium by properly arranging the fingertip contact forces. According to the mechanical advantage hypothesis, during supination or pronation torque production, fingers with longer moment arms would produce greater normal force than those with shorter moment arms. Previous studies have probed this hypothesis by investigating the force contributions of the individual fingers through systematic variations (or perturbations) of properties of the grasped handle. In the current study, we examined the applicability of this hypothesis in a paradigm wherein the thumb tangential force was constrained to a minimal constant magnitude. This was achieved by placing the thumb on a freely movable slider platform. The total mass of the handle was systematically varied by adding external loads directly below the center of mass of the handle. Our findings suggest that in the human hand, the central nervous system (CNS) adopts the principle of mechanical advantage depending on an abstract sense of challenge attached to the task situation.

Low effective mechanical advantage of giraffes’ limbs during walking reveals trade-off between limb length and locomotor performance

Giraffes (Giraffa camelopardalis) possess specialised locomotor morphology, namely elongate and gracile distal limbs. Whilst this contributes to their overall height (and enhanced feeding behaviour), we propose that the combination of long limb segments and modest muscle lever arms results in low effective mechanical advantage (EMA, the ratio of in-lever to out-lever moment arms), when compared with other cursorial mammals. To test this, we used a combination of experimentally measured kinematics and ground rection forces (GRFs), musculoskeletal modelling, and inverse dynamics to calculate giraffe forelimb EMA during walking. Giraffes walk with an EMA of 0.34 (±0.05 S.D.), with no evident association with speed within their walking gait. Giraffe EMA was markedly below the expectations extrapolated from other mammals ranging from 0.03 – 297 kg, and provides further evidence that EMA plateaus or even diminishes in mammals exceeding horse size. We further tested the idea that limb segment length is a factor which determines EMA, by modelling the GRF and muscle moment arms in the extinct giraffid Sivatherium giganteum and the other extant giraffid Okapia johnstoni. Giraffa and Okapia shared similar EMA, despite a 4-6 fold difference in body mass (Okapia EMA = 0.38). In contrast Sivatherium, sharing a similar body mass to Giraffa, had greater EMA (0.59), which we propose reflects behavioural differences, such athletic performance. Our modelling approach suggests that limb length is a determinant of GRF moment arm magnitude, and that unless muscle moment arms scale isometrically with limb length, tall mammals are prone to low EMA.Significance StatementGiraffes are the tallest living animals - using their height to access food unavailable to their competitors. It is not clear how their specialized anatomy impacts their athletic ability. We made musculoskeletal models of the forelimbs from a giraffe and two close relatives, and used motion-capture and forceplate data to measure how efficient they are when walking in a straight line. A horse for example, uses just 1 unit of muscle force to oppose 1 unit of force on the ground. Giraffe limbs however are comparatively disadvantaged – their muscles must develop 3 units of force to oppose 1 unit of force at the ground. This explains why giraffes walk and run at relatively slow speeds.

Direct and biometrical estimates of the closing force of major claws of the sand fiddler crab Leptuca pugilator (Bosc, 1801) (Decapoda: Brachyura: Ocypodidae): Support for the weakening combatant hypothesis

Many conclusions concerning the functional biology of crab claws rely upon biometrical estimates of closing force, based upon measures of muscle cross-sectional area and mechanical advantage. Fiddler crab closing force patterns show variation with body size, claw size, location of the opposing claw tips, and physiological condition, so we have measured closing force of the sand fiddler crab Leptuca pugilator (Bosc, 1801) as a function of claw size, force exerted at claw tips, and at the commonly well-developed pollex tooth. Leptuca pugilator has an elongated claw with gracile dactyl and pollex. As predicted by biometrical proportions, closing force is greater at the pollex tooth than at the claw tip. The pollex tooth does shift with increasing claw size in relative position toward the claw hinge. Mechanical advantage at the pollex tooth and dactyl tip both decline with increasing claw length. But there is no difference in slope of log closing force as a function of log claw length between the pollex position and terminus of the dactyl, which demonstrates that force exerted at the pollex tooth has no impact on proportional change in closing force with increasing claw size. The log-log slope is ~0.9, reflecting the proportionally decreasing muscle cross-sectional area and lowering mechanical advantage with increasing claw size. For both the pollex tooth and the claw tip, mechanical advantage decreases very slightly with increasing claw size, but closing force proportionally decreases with increasing claw size, supporting the weakening combatant hypothesis for this species.

Jaw shape and mechanical advantage are indicative of diet in Mesozoic mammals

Jaw morphology is closely linked to both diet and biomechanical performance, and jaws are one of the most common Mesozoic mammal fossil elements. Knowledge of the dietary and functional diversity of early mammals informs on the ecological structure of palaeocommunities throughout the longest era of mammalian evolution: the Mesozoic. Here, we analyse how jaw shape and mechanical advantage of the masseter (MAM) and temporalis (MAT) muscles relate to diet in 70 extant and 45 extinct mammals spanning the Late Triassic-Late Cretaceous. In extant mammals, jaw shape discriminates well between dietary groups: insectivores have long jaws, carnivores intermediate to short jaws, and herbivores have short jaws. Insectivores have low MAM and MAT, carnivores have low MAM and high MAT, and herbivores have high MAM and MAT. These traits are also informative of diet among Mesozoic mammals (based on previous independent determinations of diet) and set the basis for future ecomorphological studies.

Dental microwear texture analysis along reptile tooth rows: complex variation with non-dietary variables

Dental microwear texture analysis (DMTA) is a powerful technique for reconstructing the diets of extant and extinct taxa. Few studies have investigated intraspecific microwear differences along with tooth rows and the influence of endogenous non-dietary variables on texture characteristics. Sampling teeth that are minimally affected by non-dietary variables is vital for robust dietary reconstructions, especially for taxa with non-occlusal (non-chewing) dentitions as no standardized sampling strategies currently exist. Here, we apply DMTA to 13 species of extant reptile (crocodilians and monitor lizards) to investigate intraspecific microwear differences along with tooth rows and to explore the influence of three non-dietary variables on exhibited differences: (i) tooth position, (ii) mechanical advantage, and (iii) tooth aspect ratio. Five species exhibited intraspecific microwear differences. In several crocodilians, the distally positioned teeth exhibited the ‘roughest' textures, and texture characteristics correlated with all non-dietary variables. By contrast, the mesial teeth of the roughneck monitor ( Varanus rudicollis ) exhibited the ‘roughest' textures, and texture characteristics did not correlate with aspect ratio. These results are somewhat consistent with how reptiles preferentially use their teeth during feeding. We argue that DMTA has the potential to track mechanical and behavioural differences in tooth use which should be taken into consideration in future dietary reconstructions.