Modelling evolutionary tempo and mode using formal morphological spaces and Markov chain principles.

Evolutionary tempo and mode summarize ancient and controversial subjects of theoretical biology such as gradualism, convergence, contingence, trends, and entrenchment. We employed an integrative methodological approach to explore the evolutionary tempo and mode of Lepidosaurian phalangeal formulae (PFs). This approach involves quantifying the frequencies of morphological changes along an evolutionary trajectory. The five meristic characters encoded by PFs are particularly valuable in revealing evolutionary patterns, owing to their discrete nature and extensive documentation in the literature. Based on a pre-existing dataset of PFs from 649 taxa (35 Lepidosauria families, including fossils), from which there exists a unique repertoire of 53 formulations, our approach simultaneously considers phenetic and phylogenetic data. This culminates in a diagram accounting for the phylogenetic dynamic of evolution traversing across different regions of morphospace. The method involves enumerating phenotypical options, reconstructing phenotypes across the phylogeny, projecting phenotypes onto a morphospace, and constructing a flow network from the frequency of evolutionary transitions between unique phenotypic conditions. This approach links Markovian chains and evolutionary trajectories to formally define parameters that describe the underlying transitions of morphological change. Among other results, we found that (a) PF evolution exhibits a clear trend towards reduction in the phalangeal count and that (b) evolutionary change tends to occur significantly between morphologically similar PFs. Notwithstanding, although minor but not trivial, transitions between distant formulas -jumps- occur. Our results support a pluralistic view including stasis, gradualism, and saltationism discriminating their prevalence in a target character evolution.

Angiosperm flowers reached their highest morphological diversity early in their evolutionary history.

Flowers are the complex and highly diverse reproductive structures of angiosperms. Because of their role in sexual reproduction, the evolution of flowers is tightly linked to angiosperm speciation and diversification. Accordingly, the quantification of floral morphological diversity (disparity) among angiosperm subgroups and through time may give important insights into the evolutionary history of angiosperms as a whole. Based on a comprehensive dataset focusing on 30 characters describing floral structure across angiosperms, we used 1201 extant and 121 fossil flowers to measure floral disparity and explore patterns of floral evolution through time and across lineages. We found that angiosperms reached their highest floral disparity in the Early Cretaceous. However, decreasing disparity toward the present likely has not precluded the innovation of other complex traits at other morphological levels, which likely played a key role in the outstanding angiosperm species richness. Angiosperms occupy specific regions of the theoretical morphospace, indicating that only a portion of the possible floral trait combinations is observed in nature. The ANA grade, the magnoliids, and the early-eudicot grade occupy large areas of the morphospace (higher disparity), whereas nested groups occupy narrower regions (lower disparity).

Claws and toepads in mainland and island Anolis (Squamata: Dactyloidae): Different adaptive radiations with intersectional morphospatial zones.

Anolis lizards have evolved morphologies in response to different selective factors related to microhabitat use. Morphological diversity exhibits evolutionary patterns that reveal similarities and unique regional traits among the mainland and island environments and among Greater Antilles and Lesser Antilles islands. In the Greater Antilles and mainland environments anole species are classified into morphological/ecological groups, that are known as morphotypes (mainland) or ecomorphs (Greater Antilles). Morphotypes are defined only with morphological information; in contrast, for ecomorph assignment both morphology and ethology are required. For mainland species distributed in northwestern South America 10 morphotypes were proposed to include the morphological diversity of 59 species. We obtained data from body size, limbs length, tail length, and the number of lamellae for an additional ten species occurring in the same region and assigned them into morphotypes. We also collected data of the claw and toepad diversity of mainland and island Anolis from northwestern South America and compared it to the claw and toepads morphology recorded for the Greater Antilles and Lesser Antilles islands, under a phylogenetic framework. We found new island morphotypes (MT11-MT13) of Anolis from northwestern South America. When comparing claws and toepads morphology among the 13 morphotypes we found that morphological variation of these traits partially corresponds to morphotype groups. For instance, habitat specialist species like Anolis heterodermus, classified in morphotype 4 (MT4), have a characteristic design of broad toepad and reduced claws, and non-unique design of toepads and claws occurs in morphotypes MT1, MT2, MT5, MT10, and MT13. We also compared claws and toepads of fore and hindlimbs within the same individual, and found that even if limbs show differences in claws and toepads, suggesting that they perform differential biomechanical function, the degree of within individual variation is specific and not related to morphotype assignment. Our data supported the convergent and unique regional evolution among mainland and island anoles, and revealed aspects of correlative evolution of functional traits of claws and toepads that probably are related to minor differences in microhabitat use among mainland and island species, as suggested by previously published literature. Lastly, the evolutionary pattern of morphological diversity of claws and toepads of Anolis in the mainland and island environment supports both unique regional traits and common selective and historical factors that have molded Anolis morphological diversity.

Morphospace analysis leads to an evo-devo model of digit patterning.

Biological forms occupy a constrained portion of theoretical morphospaces. Developmental models accounting for empirical morphospaces are necessary to achieve a better understanding of this phenomenon. We analyzed the phalangeal formulas (PFs) in lizards and relatives' hands by comparing them with a set of simulated PFs that compose a theoretical morphospace. We detected that: (1) the empirical morphospace is severely limited in size, (2) the PFs comply with two properties of phalangeal count per digit, namely the ordering rule (DI ≤ DII ≤ DIII ≤ DIV ≥ DV), and the contiguity relationship (neighbor digits differ on average in one phalanx), (3) the totality of the PFs can be categorized into four categories of hands aligned along a feasibility gradient. We also reconstructed the evolution of PFs and found a stepwise trajectory from the plesiomorphic PF towards reduced conditions. Finally, we propose a developmental model as the generative mechanism behind the PFs. It is consistent with the bulk of evidence managed and involves an ordered digit primordia initialization timed with periodic signals of joint formation coming from digit tips. Our approach is also useful to address the study of other meristic sequences in nature such as dental, floral, and branchial formulas.

Evolutionary transition between bee pollination and hummingbird pollination in Salvia: Comparing means, variances and covariances of corolla traits.

Covariation among traits can modify the evolutionary trajectory of complex structures. This process is thought to operate at a microevolutionary scale, but its long-term effects remain controversial because trait covariation can itself evolve. Flower morphology, and particularly floral trait (co)variation, has been envisioned as the product of pollinator-mediated selection. Available evidence suggests that major changes in pollinator assemblages may affect the joint expression of floral traits and their phenotypic integration. We expect species within a monophyletic lineage sharing the same pollinator type will show not only similarity in trait means but also similar phenotypic variance-covariance structures. Here, we tested this expectation using eighteen Salvia species pollinated either by bees or by hummingbirds. Our findings indicated a nonsignificant multivariate phylogenetic signal and a decoupling between means and variance-covariance phenotypic matrices of floral traits during the evolution to hummingbird pollination. Mean trait value analyses revealed significant differences between bee- and hummingbird-pollinated Salvia species although fewer differences were detected in the covariance structure between groups. Variance-covariance matrices were much more similar among bee- than hummingbird-pollinated species. This pattern is consistent with the expectation that, unlike hummingbirds, bees physically manipulate the flower, presumably exerting stronger selection pressures favouring morphological convergence among species. Overall, we conclude that the evolution of hummingbird pollination proceeded through different independent transitions. Thus, although the evolution of hummingbird pollination led to a new phenotypic optimum, the process involved the diversification of the covariance structure.

Spatial Organization of Five-Fold Morphology as a Source of Geometrical Constraint in Biology.

A basic pattern in the body plan architecture of many animals, plants and some molecular and cellular systems is five-part units. This pattern has been understood as a result of genetic blueprints in development and as a widely conserved evolutionary character. Despite some efforts, a definitive explanation of the abundance of pentagonal symmetry at so many levels of complexity is still missing. Based on both, a computational platform and a statistical spatial organization argument, we show that five-fold morphology is substantially different from other abundant symmetries like three-fold, four-fold and six-fold symmetries in terms of spatial interacting elements. We develop a measuring system to determine levels of spatial organization in 2D polygons (homogeneous or heterogeneous partition of defined areas) based on principles of regularity in a morphospace. We found that spatial organization of five-fold symmetry is statistically higher than all other symmetries studied here (3 to 10-fold symmetries) in terms of spatial homogeneity. The significance of our findings is based on the statistical constancy of geometrical constraints derived from spatial organization of shapes, beyond the material or complexity level of the many different systems where pentagonal symmetry occurs.

A combinatorial approach to angiosperm pollen morphology.

Angiosperms (flowering plants) are strikingly diverse. This is clearly expressed in the morphology of their pollen grains, which are characterized by enormous variety in their shape and patterning. In this paper, I approach angiosperm pollen morphology from the perspective of enumerative combinatorics. This involves generating angiosperm pollen morphotypes by algorithmically combining character states and enumerating the results of these combinations. I use this approach to generate 3 643 200 pollen morphotypes, which I visualize using a parallel-coordinates plot. This represents a raw morphospace. To compare real-world and theoretical morphologies, I map the pollen of 1008 species of Neotropical angiosperms growing on Barro Colorado Island (BCI), Panama, onto this raw morphospace. This highlights that, in addition to their well-documented taxonomic diversity, Neotropical rainforests also represent an enormous reservoir of morphological diversity. Angiosperm pollen morphospace at BCI has been filled mostly by pollen morphotypes that are unique to single plant species. Repetition of pollen morphotypes among higher taxa at BCI reflects both constraint and convergence. This combinatorial approach to morphology addresses the complexity that results from large numbers of discrete character combinations and could be employed in any situation where organismal form can be captured by discrete morphological characters.

Size variation, growth strategies, and the evolution of modularity in the mammalian skull.

Allometry is a major determinant of within-population patterns of association among traits and, therefore, a major component of morphological integration studies. Even so, the influence of size variation over evolutionary change has been largely unappreciated. Here, we explore the interplay between allometric size variation, modularity, and life-history strategies in the skull from representatives of 35 mammalian families. We start by removing size variation from within-species data and analyzing its influence on integration magnitudes, modularity patterns, and responses to selection. We also carry out a simulation in which we artificially alter the influence of size variation in within-taxa matrices. Finally, we explore the relationship between size variation and different growth strategies. We demonstrate that a large portion of the evolution of modularity in the mammalian skull is associated to the evolution of growth strategies. Lineages with highly altricial neonates have adult variation patterns dominated by size variation, leading to high correlations among traits regardless of any underlying modular process and impacting directly their potential to respond to selection. Greater influence of size variation is associated to larger intermodule correlations, less individualized modules, and less flexible responses to natural selection.

Head morphology and degree of variation in lacerta bilineata: podarcis muralis and podarcis sicula / Morfología de la cabeza y el grado de variación en lacerta bilineata: podarcis muralis y podarcis sicula

The morphology of cephalic scales in Lacertids is organised in well defined geometrical structures. The variation of these elements is related to the underlying bone growth and morphogenesis, but it is also associated with the muscular system and the sutural dynamics. In this paper, the patterns of variation of the cephalic scales have been compared between three common Mediterranean species: Podarcis muralis, Podarcis sicula and Lacerta bilineata. The morphospace generated by the morphological relationships within the cephalic system in these three species is investigated in order to consider their degree of variation and their anatomical peculiarities. Generally, Lacerta is 64 percent larger than Podarcis, shows a relative reduction of the frontal scale, enlarged fronto-parietal structures, and stretched occipital area. L. bilineata shows the smaller degree of variation within the shape space, while P. muralis shows the highest values. The morphology of the two genera is definitely different mostly because of allometric variation. Non-allometric distinctions between the three species are subtle but detectable. The degree and pattern of variation are interpreted in terms of possible environmental pressures and of functional cranial dynamics associated with the fronto-parietal suture, respectively. In this sense, the structural relationships between bones and scales are of particular interest to further investigate ontogeny and phylogeny in reptiles.

La morfología de las escamas cefálicas en Lacértidos se organiza en estructuras geométricas bien definidas. La variación de estos elementos está relacionada con el crecimiento y la morfogénesis del hueso subyacente, pero está también es asociada con el sistema muscular y sutural dinámico. En este trabajo, son comparados los patrones de variación de las escamas cefálicas de tres especies mediterráneas comunes: Podarcis muralis, Podarcis sicula y Lacerta bilineata. El morfoespacio generado por las relaciones morfológicas con el sistema cefálico en estas tres especies se investigó con el fin de examinar su grado de variación y sus peculiaridades anatómicas. En general, Lacerta es 64 por ciento más grande que Podarcis, muestra una reducción relativa de la escama frontal, alargamiento de la estructura fronto-parietal, y estrechamiento del área occipital. L. bilineata muestra el menor grado de variación en la forma del espacio, mientras que P. muralis muestra los valores más altos. La morfología de los dos géneros es diferente principalmente debido a variaciones alométricas. Diferencias no alométricas entre las tres especies son sutiles pero detectables. El grado y el patrón de variación son interpretados en términos de las posibles presiones del medio ambiente y la dinámica funcional craneal asociada a la sutura fronto-parietal, respectivamente. En este sentido, las relaciones estructurales entre los huesos y las escamas son de particular interés para seguir investigando ontogenia y filogenia de los reptiles.