Allometric space and allometric disparity: a developmental perspective in the macroevolutionary analysis of morphological disparity

Here, we advance novel uses of allometric spaces--multidimensional spaces specifically defined by allometric coefficients--with the goal of investigating the focal role of development in shaping the evolution of morphological disparity. From their examination, operational measures of allometric disparity can be derived, complementing standard signals of morphological disparity through an intuitive and process-oriented refinement of established analytical protocols used in disparity studies. Allometric spaces thereby become a promising context to reveal different patterns of evolutionary developmental changes and to assess their relative prevalence and importance. Such spaces offer a novel domain of investigation of phenotypic variation and should help in detecting large-scale trends, thus placing various macroevolutionary phenomena in an explicitly developmental context. Ammonoidea (Cephalopoda) at the Lower-Middle Jurassic transition were chosen as a case study to illustrate this methodological approach. We constructed two phenotypic spaces: a static, adult one (adult morphospace) and a dynamic, developmental one (allometric space). Comparative disparity analyses show a strikingly stable occupation in both spaces, despite extensive change in taxonomic composition. In contrast, disparity analyses of subclades reveal clearly distinct morphological and allometric disparity dynamics. Allometric approaches allow developmental insights into morphological diversification otherwise intractable from the analysis of adult morphospace alone.     

Comparable disparity in the appendicular skeleton across the fish–tetrapod transition,and the morphological gap between fish and tetrapod postcrania

Appendicular skeletal traits are used to quantify changes in morphological disparity and morphospace occupation across the fish–tetrapod transition and to explore the informativeness of different data partitions in phylogeny reconstruction. Anterior appendicular data yield trees that differ little from those built from the full character set, whilst posterior appendicular data result in considerable loss of phylogenetic resolution and tree branch rearrangements. Overall, there is a significant incongruence in the signals associated with pectoral and pelvic data. The appendicular skeletons of fish and tetrapods attain similar levels of morphological disparity (at least when data are rarefied at the maximum sample size for fish in our study) and occupy similarly sized regions of morphospace. However, fish appear more dispersed in morphospace than tetrapods do. All taxa show a heterogeneous distribution in morphospace, and there is a clear separation between fish and tetrapods despite the presence of several evolutionarily intermediate taxa.     

Inferring the accumulation of morphological disparity in epiphyllous liverworts

Phylogenetic studies of lineages growing in extreme environments have frequently recovered evidence not only of high level of homoplasy but also of discordance of morphological disparity and species diversity. It has been suggested that this divergence may be caused by developmental constraints and/or natural selection. Here we explored these hypotheses by inferring the phenotypic evolution of the derived liverwort genus Cololejeunea. These liverworts occur preferentially on the surface of leaves or other aerial parts of vascular plants growing in wet forests. The evolution of 12 morphological characters was studied using a phylogenetic framework comprising 70 species of Cololejeunea. The phylogeny was reconstructed using DNA sequences of one nuclear and two plastid regions and enabled the inference of the evolution of the studied morphological characters by determining the frequency of homoplasy. Mantel tests were used to test for correlations of morphological disparity?×?species diversity and morphological disparity?×?epiphytism. The phylogenetic informativeness of each binary character was estimated by the D metric of the Fritz and Purvis test, and the relationship between each character and epiphytism was inferred by Pearson’s coefficient. We evaluated the morphospace occupation using principal coordinate analyses. Our results not only recovered high levels of homoplasy but also weak correlations of morphological disparity and species diversity. Morphological disparity was not linked to epiphytism, although positive or negative relationships between some characters and epiphytism were found. The Brownian model of character evolution was not rejected for the studied morphological disparity in Cololejeunea with the exception of asexual propagules. The observations support the prediction that iterative evolution in a well-defined morphospace may result in rampant homoplasy and the observed divergence of disparity and diversity.     

Categorical versus geometric morphometric approaches to characterizing the evolution of morphological disparity in Osteostraci (Vertebrata,stem Gnathostomata)

Morphological variation (disparity) is almost invariably characterized by two non-mutually exclusive approaches: (1) quantitatively, through geometric morphometrics; and (2) in terms of discrete, ‘cladistic’, or categorical characters. Uncertainty over the comparability of these approaches diminishes the potential to obtain nomothetic insights into the evolution of morphological disparity and the few benchmarking studies conducted so far show contrasting results. Here, we apply both approaches to characterizing morphology in the stem-gnathostome clade Osteostraci in order to assess congruence between these alternative methods as well as to explore the evolutionary patterns of the group in terms of temporal disparity and the influence of phylogenetic relationships and habitat on morphospace occupation. Our results suggest that both approaches yield similar results in morphospace occupation and clustering, but also some differences indicating that these metrics may capture different aspects of morphology. Phylomorphospaces reveal convergence towards a generalized ‘horseshoe’-shaped cranial morphology and two strong trends involving major groups of osteostracans (benneviaspidids and thyestiids), which probably reflect adaptations to different lifestyles. Temporal patterns of disparity obtained from categorical and morphometric approaches appear congruent, however, disparity maxima occur at different times in the evolutionary history of the group. The results of our analyses indicate that categorical and continuous data sets may characterize different patterns of morphological disparity and that discrepancies could reflect preservational limitations of morphometric data and differences in the potential of each data type for characterizing more or less inclusive aspects of overall phenotype.     

The complex effects of mass extinctions on morphological disparity

Studies of biodiversity through deep time have been a staple for biologists and paleontologists for over 60 years. Investigations of species richness (diversity) revealed that at least five mass extinctions punctuated the last half billion years, each seeing the rapid demise of a large proportion of contemporary taxa. In contrast to diversity, the response of morphological diversity (disparity) to mass extinctions is unclear. Generally, diversity and disparity are decoupled, such that diversity may decline as morphological disparity increases, and vice versa. Here, we develop simulations to model disparity changes across mass extinctions using continuous traits and birth-death trees. We find no simple null for disparity change following a mass extinction but do observe general patterns. The range of trait values decreases following either random or trait-selective mass extinctions, whereas variance and the density of morphospace occupation only decline following trait-selective events. General trends may differentiate random and trait-selective mass extinctions, but methods struggle to identify trait selectivity. Long-term effects of mass extinction trait selectivity change support for phylogenetic comparative methods away from the simulated Brownian motion toward Ornstein-Uhlenbeck and Early Burst models. We find that morphological change over mass extinction is best studied by quantifying multiple aspects of morphospace occupation.     

Evolution of Cranial Shape in Caecilians (Amphibia: Gymnophiona)

Insights into morphological diversification can be obtained from the ways the species of a clade occupy morphospace. Projecting a phylogeny into morphospace provides estimates of evolutionary trajectories as lineages diversified information that can be used to infer the dynamics of evolutionary processes that produced patterns of morphospace occupation. We present here a large-scale investigation into evolution of morphological variation in the skull of caecilian amphibians, a major clade of vertebrates. Because caecilians are limbless, predominantly fossorial animals, diversification of their skull has occurred within a framework imposed by the functional demands of head-first burrowing. We examined cranial shape in 141 species, over half of known species, using X-ray computed tomography and geometric morphometrics. Mapping an existing phylogeny into the cranial morphospace to estimate the history of morphological change (phylomorphospace), we find a striking pattern: most species occupy distinct clusters in cranial morphospace that closely correspond to the main caecilian clades, and each cluster is separated by unoccupied morphospace. The empty spaces in shape space are unlikely to be caused entirely by extinction or incomplete sampling. The main caecilian clades have different amounts of morphological disparity, but neither clade age nor number of species account for this variation. Cranial shape variation is clearly linked to phyletic divergence, but there is also homoplasy, which is attributed to extrinsic factors associated with head-first digging: features of caecilian crania that have been previously argued to correlate with differential microhabitat use and burrowing ability, such as subterminal and terminal mouths, degree of temporal fenestration (stegokrotaphy/zygokrotaphy), and eyes covered by bone, have evolved and many combinations occur in modern species. We find evidence of morphological convergence in cranial shape, among species that have eyes covered by bone, resulting in a narrow bullet-shaped head. These results reveal a complex history, including early expansion of morphospace and both divergent and convergent evolution resulting in the diversity we observe today.     

A null model of morphospace occupation

Progress in understanding the relationship between lineage diversity, morphological diversity, and morphospace dynamics has been hampered by the lack of an appropriate null model of morphospace occupation. In this article, we introduce a simple class of models based on branching random walks (BRWs) for continuous traits. We show that many of the observed patterns of morphospace occupation might be simply a consequence of the dynamics of BRWs and therefore might not require special explanations. We also provide expected patterns of morphospace occupation according to a number of different conditions. In particular, we model BRWs on neutral landscapes and demonstrate that clumping in morphospace is possible even in the absence of adaptive landscapes with well-defined peaks and valleys. The quantitative definition of the BRW provides a means to analyze, both computationally and analytically, patterns of morphospace occupation according to different hypotheses.     

Patterns of cranial ontogeny in lacertid lizards: morphological and allometric disparity

We explored the ontogenetic dynamics of the morphological and allometric disparity in the cranium shapes of twelve lacertid lizard species. The analysed species (Darevskia praticola, Dinarolacerta mosorensis, Iberolacerta horvathi, Lacerta agilis, L. trilineata, L. viridis, Podarcis erhardii, P. melisellensis, P. muralis, P. sicula, P. taurica and Zootoca vivipara) can be classified into different ecomorphs: terrestrial lizards that inhabit vegetated habitats (habitats with lush or sparse vegetation), saxicolous and shrub‐climbing lizards. We observed that there was an overall increase in the morphological disparity (MD) during the ontogeny of the lacertid lizards. The ventral cranium, which is involved in the mechanics of jaw movement and feeding, showed higher levels of MD, an ontogenetic shift in the morphospace planes and more variable allometric patterns than more conserved dorsal crania. With respect to ecology, the allometric trajectories of the shrub‐climbing species tended to cluster together, whereas the allometric trajectories of the saxicolous species were highly dispersed. Our results indicate that the ontogenetic patterns of morphological and allometric disparity in the lacertid lizards are modified by ecology and functional constraints and that the identical mechanisms that lead to intraspecific morphological variation also produce morphological divergence at higher taxonomic levels.     

DISPARITY: MORPHOLOGICAL PATTERN AND DEVELOPMENTAL CONTEXT

Abstract:  The distribution of organic forms is clumpy at any scale from populations to the highest taxonomic categories, and whether considered within clades or within ecosystems. The fossil record provides little support for expectations that the morphological gaps between species or groups of species have increased through time as it might if the gaps were created by extinction of a more homogeneous distribution of morphologies. As the quantitative assessments of morphology have replaced counts of higher taxa as a metric of morphological disparity, numerous studies have demonstrated the rapid construction of morphospace early in evolutionary radiations, and have emphasized the difference between taxonomic measures of morphological diversity and quantitative assessments of disparity. Other studies have evaluated changing patterns of disparity across mass extinctions, ecomorphological patterns and the patterns of convergence within ecological communities, while the development of theoretical morphology has greatly aided efforts to understand why some forms do not occur. A parallel, and until recently, largely separate research effort in evolutionary developmental biology has established that the developmental toolkit underlying the remarkable breadth of metazoan form is largely identical among Bilateria, and many components are shared among all metazoa. Underlying this concern with disparity is a question about temporal variation in the production of morphological innovations, a debate over the relative significance of the generation of new morphologies vs. differential probabilities of their successful introduction, and the relative importance of constraint, convergence and contingency in the evolution of form.     

早期生命形态演化研究中的定量方法

定量古生物学是现代古生物学的一个分支,提倡用定量的手段来研究地质历史时期生命的演化过程。我国从事定量古生物研究的群体较小,特别是对前寒武纪早期生命演化的定量研究还没有系统地展开。这篇文章将主要介绍如何利用定量手段来研究前寒武纪化石的形态演化。对于前寒武纪化石,由于大部分化石分类属性的不确定性,通常使用几何性状对化石的最基本形态结构进行分析,并用存在/缺失(1/0)这种离散变量对每个性状进行量化。非参数多维标量分析方法[Non-parametric multidimensional scaling analysis(MDS)]可以将高维度的离散数据投影到二维或者三维的形态空间上,进而探讨生物群在形态空间中所占有的范围;由离散变量计算得出的生物群的表形分异度(morphological disparity)可以用MDS方差或者平均差异参数[Mean dissimilarity coeffi-cient(MDC)]来计算。形态空间的范围(morphospace range)和表形分异度是相互联系的,如果形态空间范围是固定的,那么表形分异度实际上代表了生物群在形态空间中的分布密度。在解释数据之前,需要对可能存在的样本效应进行测试。常用的方法包括稀释法(rarefaction)、随机取样法(randomization)和自举法(bootstrapping)等。为了帮助读者进一步了解这些方法的使用,文中列举了三个实例:伊迪卡拉生物的形态演化,元古代宏观藻类的形态演化和元古代及寒武纪疑源类的演化。     

Disparity Changes in 370 Ma Devonian Fossils: The Signature of Ecological Dynamics?

Early periods in Earth's history have seen a progressive increase in complexity of the ecosystems, but also dramatic crises decimating the biosphere. Such patterns are usually considered as large-scale changes among supra-specific groups, including morphological novelties, radiation, and extinctions. Nevertheless, in the same time, each species evolved by the way of micro-evolutionary processes, extended over millions of years into the evolution of lineages. How these two evolutionary scales interacted is a challenging issue because this requires bridging a gap between scales of observation and processes. The present study aims at transferring a typical macro-evolutionary approach, namely disparity analysis, to the study of fine-scale evolutionary variations in order to decipher what processes actually drove the dynamics of diversity at a micro-evolutionary level. The Late Frasnian to Late Famennian period was selected because it is punctuated by two major macro-evolutionary crises, as well as a progressive diversification of marine ecosystem. Disparity was estimated through this period on conodonts, tooth-like fossil remains of small eel-like predators that were part of the nektonic fauna. The study was focused on the emblematic genus of the period, Palmatolepis. Strikingly, both crises affected an already impoverished Palmatolepis disparity, increasing risks of random extinction. The major disparity signal rather emerged as a cycle of increase and decrease in disparity during the inter-crises period. The diversification shortly followed the first crisis and might correspond to an opportunistic occupation of empty ecological niche. The subsequent oriented shrinking in the morphospace occupation suggests that the ecological space available to Palmatolepis decreased through time, due to a combination of factors: deteriorating climate, expansion of competitors and predators. Disparity changes of Palmatolepis thus reflect changes in the structure of the ecological space itself, which was prone to evolve during this ancient period where modern ecosystems were progressively shaped.     

Phylogenetic and size constrains on cranial ontogenetic allometry of spiny rats (Echimyidae,Rodentia)

Analysis of ontogenetic development is crucial for understanding the emergence of phenotypic discrepancies between animal taxa. The study of allometric trajectories within a phylogenetic context is a feasible approach to assess the morphological change across different evolutionary lineages. Here, we report the disparity of multivariate ontogenetic allometry in the Echimyidae, a taxonomically diverse rodent family, as well as the effects of size on the evolution of skull ontogeny. The ontogenetic trajectories of 15 echimyid operational taxonomic unities (12 genera plus one genus with three species) belonging to all subfamilies and major clades, when plotted in allometric space, revealed strong and significant phylogenetic signals. Allometric trajectories were found to be constrained by phylogenetic ancestry, with changes approximately adjusting to a Brownian motion model of evolution. Moreover, the occupation of allometric space by echimyid taxa was significantly correlated with adult size rather than with shape, suggesting that the variation in adult size might result in critically intrinsic and structural constraints on allometric coefficients. These findings disagreed with the hypothesis that allometric disparities might be mainly adaptive with undetectable phylogenetic signals.     

Bathymetric patterns of morphological disparity in deep-sea gastropods from the western North Atlantic basin

Understanding patterns of species richness requires knowledge of the individual roles species play in community structure. Here, I use gastropod shells as a source of information about both their ecological and their evolutionary functions in generating bathymetric gradients of diversity. Specifically, morphological disparity of shell architecture in deep-sea gastropods is evaluated over a depth gradient in the western North Atlantic by constructing an empirical morphospace based on an eigenshape analysis. Morphological disparity is quantified by calculating the centroid, total range, and dispersion of the morphospace at each station along the depth gradient. The results indicate that local faunas are drawn from a regional pool with the same variance but that average dissimilarity in forms reflects the number of species in the sample. The range of the morphospace at local scales is also less than at regional scales, resulting from the variability of the morphospace centroid over depth. Although the position of the morphospace changes with depth, morphological disparity remains unaffected. Despite the lack of bathymetric patterns in variance, patterns in nearest neighbor distance persist. The findings suggest the importance of interacting ecological and evolutionary processes at varying spatiotemporal scales for both morphological disparity and species richness.     

Morphological integration and developmental progress during fish ontogeny in two contrasting habitats

SUMMARY Morphological integration can respond to environmental conditions, a response that may be dynamic through ontogeny. Among fishes, brook charrs ( Salvelinus fontinalis ) display a trophic polymorphism that makes it a good species for analyzing the ontogeny of morphological integration. To better understand the processes regulating variation and integration, we assess the ontogenetic dynamics of covariances and developmental progress for populations of S. fontinalis from two habitats that differ in water velocity; lake and stream. Geometric morphometrics and developmental progress were evaluated on 751 and 198 specimens, respectively. In both habitats, most ossification events occur before the transition from alevin to juvenile. This threshold defines two distinct periods. During the first period representing free-embryos and alevins, there are important shape changes and rapid ossification, integration tends to be relatively low and decreasing and the variance of shape drastically decreases. During the juvenile period, the rate of shape change decreases and the onset of ossification is nearly complete, plus integration increases and shape variance stabilizes. While we find two distinct developmental periods, we nonetheless find a notable stability underlying the ontogenetic dynamics of variability as well as gradual change in the structure of covariation within each habitat. Our results imply that the variability of juvenile body shape does not seem to retain signals of variability determined early in ontogeny and warrants caution in using juvenile as guides to the earlier causes of variability. Overall, this study highlights the difficulty of inferring causes of integration from studies of static covariance.     

Tempo and mode in the evolution of morphological disparity in the Neotropical fern genus Pleopeltis

Species diversity and morphological disparity are two measures to examine the diversity of life. Evidence based on the fossil record suggests a complex relation between these two parameters of biodiversity including frequent decoupling of their assembly through time. However, rather few studies explored the correlation of these two measurements by studying extant plant species. This study was designed to explore the accumulation of morphological disparity of the derived Neotropical fern genus Pleopeltis. To explore the relationship of species diversity and morphological disparity, we employed several approaches including divergence time estimates based on DNA sequence variation, reconstruction of character state changes based on a morphological matrix comprising 41 discrete characters, and exploration of the phylomorphospace. Accumulation of species diversity and morphological disparity was found to be concordant although the assumption of independence was not rejected for the accumulation of genetic and morphological variation. The phylomorphospace reconstruction provided further evidence for clade‐specific morphospace expansion that imply developmental pathways and competition among clades as major factors shaping the assembly of morphological disparity over time.     

Diversity trends and their ontogenetic basis: an exploration of allometric disparity in rodents

It has been hypothesized that most morphological evolution occurs by allometric differentiation. Because rodents encapsulate a phenomenal amount of taxonomic diversity and, among several clades, contrasting levels of morphological diversity, they represent an excellent subject to address the question: how variable are allometric patterns during evolution? We investigated the influence of phylogenetic relations and ecological factors on the results of the first quantification of allometric disparity among rodents by exploring allometric space, a multivariate morphospace here derived from, and encapsulating all, the ontogenetic trajectories of 34 rodent species from two parallel phylogenetic radiations. Disparity was quantified using angles between ontogenetic trajectories for different species and clades. We found an overlapping occupation of allometric space by muroid and hystricognath species, revealing both clades possess similar abilities to evolve in different directions of phenotypic space, and anatomical diversity does not act to constrain the labile nature of allometric patterning. Morphological features to enable efficient processing of food serve to group rodents in allometric space, reflecting the importance of convergent morphology, rather than shared evolutionary history, in the generation of allometric patterns. Our results indicate that the conserved level of morphological integration found among primates cannot simply be extended to all mammals.     

GEOMETRIC MORPHOMETRICS OF THE SKULL ROOF OF STEREOSPONDYLS (AMPHIBIA: TEMNOSPONDYLI)

Abstract:  Geometric morphometric analysis using relative warps is applied to the skull roof of 62 species of stereospondyls and their closest outgroups (i.e. basal archegosauriforms) from among temnospondyl amphibians. Twenty-one landmarks and five taxonomic groups are used for comparisons. Their skull evolution is quantified in a morphospace defined by two relative warps axes. The majority of groups show poor concordance between morphological and phylogenetic distances. The only exception is represented by Yates and Warren's study of stereospondyl relationships, in which concordance is high. Only basal archegosauriforms and rhinesuchids show significant overlap in morphospace, although this might be due to low sample sizes. Regression of estimated mean disparity against taxon sample size shows that species within both the trematosauroid and the rhytidostean groups are more widely dispersed in morphospace than species belonging to any of the remaining stereospondyl groups. Stereospondyl skull evolution was characterized by divergence between major clades and convergence within those clades. Changes in patterns of morphospace occupation through time agree with the hypothesis of an 'explosive' radiation in the early Early Triassic, after the extinction of basal archegosauriforms at the end of the Permian.     

EXTINCTION SPACE—A METHOD FOR THE QUANTIFICATION AND CLASSIFICATION OF CHANGES IN MORPHOSPACE ACROSS EXTINCTION BOUNDARIES

Three main modes of extinction are responsible for reductions in morphological disparity: (1) random (caused by a nonselective extinction event); (2) marginal (a symmetric, selective extinction event trimming the margin of morphospace); and (3) lateral (an asymmetric, selective extinction event eliminating one side of the morphospace). These three types of extinction event can be distinguished from one another by comparing changes in three measures of morphospace occupation: (1) the sum of range along the main axes; (2) the sum of variance; and (3) the position of the centroid. Computer simulations of various extinction events demonstrate that the pre‐extinction distribution of taxa (random or normal) in the morphospace has little influence on the quantification of disparity changes, whereas the modes of the extinction events play the major role. Together, the three disparity metrics define an “extinction‐space” in which different extinction events can be directly compared with one another. Application of this method to selected extinction events (Frasnian‐Famennian, Devonian‐Carboniferous, and Permian‐Triassic) of the Ammonoidea demonstrate the similarity of the Devonian events (selective extinctions) but the striking difference from the end‐Permian event (nonselective extinction). These events differ in their mode of extinction despite decreases in taxonomic diversity of similar magnitude.     

Testing the evolutionary constraints of metamorphosis: The ontogeny of head shape in Triturus newts

In vertebrates with complex, biphasic, life cycles, larvae have a distinct morphology and ecological preferences compared to metamorphosed juveniles and adults. In amphibians, abrupt and rapid metamorphic changes transform aquatic larvae to terrestrial juveniles. The main aim of this study is to test whether, relative to larval stages, metamorphosis (1) resets the pattern of variation between ontogenetic stages and species, (2) constrains intraspecific morphological variability, and (3) similar to the “hour‐glass” model reduces morphological disparity. We explore postembryonic ontogenetic trajectories of head shape (from hatching to completed metamorphosis) of two well‐defined, morphologically distinct Triturus newts species and their F1 hybrids. Variation in head shape is quantified and compared on two levels: dynamic (across ontogenetic stages) and static (at a particular stage). Our results show that the ontogenetic trajectories diverge early during development and continue to diverge throughout larval stages and metamorphosis. The high within‐group variance and the largest disparity level (between‐group variance) characterize the metamorphosed stage. Hence, our results indicate that metamorphosis does not canalize head shape variation generated during larval development and that metamorphosed phenotype is not more constrained relative to larval ones. Therefore, metamorphosis cannot be regarded as a developmental constraint, at least not for salamander head shape.