Evolutionary Biology

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Phylogeny with clade representatives. Phylogeny based on Kallal et al. (2021b). Major clades highlighted: Opisthothelae, grey; Mygalomorphae, brown; Synspermiata, blue; Palpimanoidea, green; UDOH Grade, orange; RTA Clade, violet; Araneoidea, red. Sclerite color code: carapace, yellow; paturons, magenta and green; fangs, blue and violet. Circles at branch terminals correspond to spider size (carapace width) (Color figure online)
Morphospace plots highlighting shape differences in spiders capturing prey aided by adhesive webs or not. A Carapace, B paturon, C fang. Shapes correspond to major spider lineages. Shape color code: predation type absent, black; predation type present, red. Landmarked surfaces correspond to structures at the extremes of the first two principal components (Color figure online)
Disparity comparisons by structure and predation mode. A Area metric of disparity based on sum of variances. B Location metric of disparity based on median of centroids. Dotted lines connect compared shape spaces as in Fig. 2. NF non-foraging web; F foraging web; NA non-adhesive web; A adhesive web; NO non-orb-web; O orb-web. Shapes code: carapace, circle; paturon, square; fang, triangle. Color code: web type absent, grey; web type present, black (Color figure online)
  • Robert J. KallalRobert J. Kallal
  • Hannah M. WoodHannah M. Wood
Understanding complex morphological shape differences has been revolutionized by the marriage of three-dimensional morphometric techniques and micro-computed tomography scanning. In animals, a major focus of this work has been the vertebrates, particularly the axial skeleton, while shape diversity in arthropods, by comparison, is less well explored. For example, the chelicerae (fanged, jaw-like mouthpart appendages) of spiders exhibit a wide degree of variation and may be expected to differ across the diversity of spider sizes and hunting strategies (e.g., active hunters versus relying on a web to intercept and capture prey) as well as in comparison to other structures on the same organism. We characterize and quantify the shapes of the carapace and chelicerae of 40 spiders across the spider tree of life and look for differences based on how those spiders attain their prey and whether their shapes coevolved or are modular. We found evidence for differences in cheliceral shape and related structures in spiders with different predation strategies as well as evidence for both integration and modularity in those structures. This suggests different pressures on the chelicerae including but not limited to predation mode. Furthermore, while differences in the structures were observed, they still must work in concert.
Over several generations of evolutionary and developmental biologists, ever since Olson and Miller’s pioneering work of the 1950’s, the concept of “morphological integration” as applied to Gaussian representations $$N(\mu ,\Sigma )$$ N ( μ , Σ ) of morphometric data has been a focus equally of methodological innovation and methodological perplexity. Reanalysis of a century-old example from Sewall Wright shows how some fallacies of distance analysis by correlations can be avoided by careful matching of the distance rosters involved to a different multivariate approach, factor analysis. I reinterpret his example by restoring the information (means and variances) ignored by the correlation matrix, while confirming what Wright called “special size factors” by a different technique, inspection of the concentration matrix $$\Sigma ^{-1}.$$ Σ - 1 . In geometric morphometrics (GMM), data accrue instead as Cartesian coordinates of labelled points; nevertheless, just as in the Wright example, statistical manipulations do better when they reconsider the normalizations that went into the generation of those coordinates. Here information about both $$\mu $$ μ and $$\Sigma ,$$ Σ , the means and the variances/covariances, can be preserved via the Boas coordinates (Procrustes shape coordinates without the size adjustment) that protect the role of size per se as an essential explanatory factor while permitting the analyst to acknowledge the realities of animal anatomy and its trajectories over time or size in the course of an analysis. A descriptive quantity for this purpose is suggested, the correlation of vectorized $$\mu $$ μ against the first eigenvector of $$\Sigma $$ Σ for the Boas coordinates. The paper reanalyzes two GMM data sets from this point of view. In one, the classic Vilmann rodent neurocranial growth data, a description of integration can be aligned with the purposes of evolutionary and developmental biology by a graphical exegesis based mainly in the loadings of the first Boas principal component. There results a multiplicity of morphometric patterns, some homogeneous and others characterized by gradients. In the other, a Vienna data set comprising human midsagittal skull sections mostly sampled along curves, a further integrated feature emerges, thickening of the calvaria, that requires a reparametrization and a modified thin plate spline graphic distinct from the digitized configurations per se. This new GMM protocol fulfills the original thrust of Olson & Miller’s (Evolution 5:325–338, 1951) “ $$\rho $$ ρ F-groups,” the alignment of statistical and biological explanatory guidance, while respecting the enormously greater range of morphological descriptors afforded by well-designed landmark/semilandmark configurations.
The multiple species hypothesis of Paul et al. (2022) presented as a a dendrogram showing specimens, taxa, synapomorphies, and autapomorphies; and b a phylogeny showing the stratigraphic ranges of the taxa as ellipses, and the speciation modes of cladogenesis and anagenesis overlaid on the stratigraphic framework of the Hell Creek Formation. Paul et al. (2022) did not independently test the trichotomy hypothesis by a numerical cladistic analysis; although the dendrogram drafted here is an arrangement it does accurately reflect the subjective schema of those authors. Specimens shown are limited to those in public trusts. Asterisks indicate type specimens
Comparison of the skulls of T. rex (right) and Ta. bataar (left) showing several species differences in the supraorbital process (a) and rostral ramus (b) of the lacrimal, horizontal ramus of the maxilla (c), ventral ramus of the prefrontal (d), and maxillary (e) and dentary (f) tooth counts. See text and Table 1 for details
Results of hierarchical clustering analysis, including a a dendrogram recovered through UPGMA agglomerative hierarchical clustering of femoral robusticity values from Paul et al. (2022); b an analogous dendrogram recovered through clustering analysis of dentary tooth ratio data; c a gap statistic plot showing the optimal number of clusters to describe femoral robusticity; d a gap statistic plot similarly showing the optimal number of clusters for describing tooth ratios. The taxonomy proposed by Paul et al. (2022) is generally similar to these results, although T. rex and ‘T. imperator’ do not form distinct morphological clusters, and clusters are not congruent between the proposed diagnostic characters. The gap statistic plots both indicate that a one-cluster model is the best supported
Histogram and density function describing the range of intraspecific variation seen in modern theropods and four tyrannosaurids. The vertical dotted line corresponds to the variation in robusticity seen in T. rex, which is well within the range of variation seen in living birds; the dark curve is the kernel density
The mesial end of the tooth row of the right dentary of the holotype of T. rex (CM 9380) showing the divot that represents the bone-filled first dentary alveolus
The Late Cretaceous dinosaur Tyrannosaurus rex was recently split into three species based on the premise that variation in the T. rex hypodigm is exceptional, indicating cryptic species and “robust” and “gracile” morphs. The morphs are based on proportional ratios throughout the skeleton. The species are claimed to be stratigraphically separate, with an early robust species followed by robust and gracile descendants. There are problems with the hypothesis: the taxon diagnoses are based on two features that overlap between the species; several skulls cannot be identified based on the diagnoses; proportional comparisons between Tyrannosaurus and other theropods are based on incomparable samples; the tooth data are problematic; the stratigraphic framework divides the Hell Creek Formation into thirds, without the stratigraphic position of each specimen, or independent age control showing the subdivisions are coeval over the entire geographic area; previous work found variation in T. rex , but it cannot be parsed into discrete categories. We tested for “gracile” and “robust” morphs by analyzing the femoral and tooth ratios that were published in the multiple species study using agglomerative hierarchical clustering. The results found that each set of ratios are explained by one cluster, showing that dimorphism is not supported. We tested for exceptional variation of the femoral ratio of Tyrannosaurus ; we calculated the mean intraspecific robusticity for 112 species of living birds and 4 nonavian theropods. The results showed that the absolute variation in Tyrannosaurus is unexceptional and it does not indicate cryptic diversity. We conclude that “ T. regina ” and “ T. imperator ” are subjective junior synonyms of T. rex .
Map showing the geographic context of this study. Yellow circles denote continental populations and species, while red circles denote island populations and species. The inset is a close-up of the islands in the Gulf of California (sensu stricto) (Color figure online)
Top left: phylorate plot for the diversification of Phyllodactylus with a Birth–death model (cool colors = slow, warm = fast). Top right: phylorate plot showing the evolutionary rates of body size along each branch of the Phyllodactylus phylogeny (cool colors = slow, warm = fast; roman numerals indicate each major clade). Note four lineages belonging to clade I present the maximum rates of evolution of body size. Bottom: Curves are kernel density plots depicting posterior probability distribution of absolute tip rates (speciation λ, extinction μ, and body size evolution β) as estimated by BAMM (Color figure online)
Top: Plot of Phyllodactylus data scaled into two PCA dimensions and color coded according to the results of K-means clustering. Bottom: Dissimilarity dendrogram resulting from hierarchical clustering of Phyllodactylus data (cluster = complete). P. delcampi represents morphotype M1 (red), P. unctus and P. paucituberculatus represent morphotype M2, while the rest of the taxa belong to morphotype M3 (black) (Color figure online)
Disparity-through-time (DTT) plots for a body size, b body traits, and c head traits. Disparity profiles are indicated by solid black lines, average Brownian-Motion simulation by dashed black lines, and 95% confidence intervals from 10,000 BM simulations by the blue polygons (Color figure online)
Empirical studies have shown that several taxa exhibit a decoupled relationship between lineage species diversification (the balance between speciation and extinction) and phenotypic diversification. This has been recognized by some authors as fundamental evidence for non-adaptive radiation. In the leaf-toed geckos Phyllodactylus of North America, there is a wide inter-specific overlap of phenotypic traits and high intra-specific morphological variation, despite predominantly allopatric distributions and the colonization of both insular and continental habitats. Here we demonstrate two outstanding aspects of the evolution of Phyllodactylus-first, that the radiation occurred with rate decoupling (body size and diversification), and second, that the contributions of island colonizations to the genus' diversification (phenotypic and species) have been of the same magnitude as those of continental habitats. Phyllodactylus diversification has proceeded with minimal ecological influence, as suggested by the identification of limited phenotypic diversity, evidenced by the wide representation of one morphotype (shared in island and mainland environments) and limited disparity (body size and shape) for long periods of time. Conversely, some head traits like snout length have increased in disparity in recent times. Most likely, snout length is being shaped by selective pressures associated with the differential exploitation of insular and continental trophic niches. The decoupling of rates (diversification and body size evolution), long periods of morphological stasis (body size and shape), overlapping of traits in the morphological space, and minimal ecological influence on the evolution of body size suggest that Phyllodactylus has proliferated following the tempo and mode of a non-adaptive radiation.
Differences in apparent evolvability in the major sea-urchin clades, portrayed in a phylomorphospace based on principal coordinates analysis of a character matrix. Modified after Hopkins and Smith (2015), used by permission (Color figure online)
Breaking bilateral symmetry in bivalves. A Cretaceous rudist Radiolites angeiodes showing disparate left (now upper) and right (now lower) valve (after Skelton, 1979, used by permission). B Eocene Caestocorbula praeviator, living within sediment with larger and more heavily ornamented left valve downward (from Beu & Raine, 2009). C extant scallop Cyclopecten hoskynsi, left valve above, right valve below (from Dijkstra et al., 2009). D Coiled Jurassic oyster Gryphaea arcuata, living with left valve downward on soft seafloor (from Seilacher, 1984). E Helically coiled Cretaceous oyster Ilymatogyra arietina, living with left valve downward on soft seafloor (from Roemer, 1862)
Evolution in diversity-disparity space. Left: Type 1—Morphology outstrips taxonomic diversification, Type 2—Morphology concordant with taxonomic diversification, Type 3—Morphology trails behind taxonomic diversification. Right, three empirical trajectories, for Cambrian-Ordovician blastozan echinoderms, Jurassic-Cretaceous aporrhaid gastropods, and Ordovician-Carboniferous blastoidean echinoderms. From Jablonski (2017b), which cites sources (Color figure online)
Evolvability is best addressed from a multi-level, macroevolutionary perspective through a comparative approach that tests for among-clade differences in phenotypic diversification in response to an opportunity, such as encountered after a mass extinction, entering a new adaptive zone, or entering a new geographic area. Analyzing the dynamics of clades under similar environmental conditions can (partially) factor out shared external drivers to recognize intrinsic differences in evolvability, aiming for a macroevolutionary analog of a common-garden experiment. Analyses will be most powerful when integrating neontological and paleontological data: determining differences among extant populations that can be hypothesized to generate large-scale, long-term contrasts in evolvability among clades; or observing large-scale differences among clade histories that can by hypothesized to reflect contrasts in genetics and development observed directly in extant populations. However, many comparative analyses can be informative on their own, as explored in this overview. Differences in clade-level evolvability can be visualized in diversity-disparity plots, which can quantify positive and negative departures of phenotypic productivity from stochastic expectations scaled to taxonomic diversification. Factors that evidently can promote evolvability include modularity—when selection aligns with modular structure or with morphological integration patterns; pronounced ontogenetic changes in morphology, as in allometry or multiphase life cycles; genome size; and a variety of evolutionary novelties, which can also be evaluated using macroevolutionary lags between the acquisition of a trait and phenotypic diversification, and dead-clade-walking patterns that may signal a loss of evolvability when extrinsic factors can be excluded. High speciation rates may indirectly foster phenotypic evolvability, and vice versa. Mechanisms are controversial, but clade evolvability may be higher in the Cambrian, and possibly early in the history of clades at other times; in the tropics; and, for marine organisms, in shallow-water disturbed habitats.
Radical shifts in reproductive systems result in radical changes in selective pressures acting on reproductive traits. Nematode Caenorhabditis elegans constitutes one of rare model systems where such shifts can be experimentally induced, providing an opportunity for studying the evolution of reproductive phenotypes in real time. Evolutionary history of predominantly selfing reproduction in has led to degeneration of traits involved outcrossing, making it inefficient. Here, we introduced obligatory outcrossing into isogenic lines of C. elegans and allowed replicate populations to evolve under the new reproductive system. We predicted that they should evolve higher outcrossing efficiency, leading to increased fitness relative to unevolved ancestors. To test this prediction, we assayed fitness of both ancestral and evolved outcrossing populations. To control for the potentially confounding effect of adaptation to laboratory conditions, we also assayed populations with wild-type (selfing) reproductive system. In five experimental blocks, we measured competitive fitness of 12 evolved populations (6 outcrossing, 6 selfing) after ca. 95 generations of evolution, along with their respective ancestors. On average, we found that fitness increased by 0.72 SD (± 0.3 CI) in outcrossing and by 0.52 (± 0.35 CI) in selfing populations, suggesting further adaptation to laboratory conditions in both types. Contrary to predictions, fitness increase was not significantly higher in outcrossing populations, suggesting no detectable adaptation to the changed reproductive system. Importantly, the results for individual populations varied strongly between experimental blocks, in some cases even differing in effect direction. This emphasises the importance of experimental replication in avoiding reporting false findings.
Experimental timelines A–C of the behavioural tests for rats experienced an exposure of anoxia and/or dexamethasone on PD2. A The neonatally-exposed rats were tested in the EPM test on PD113-114 only. No other tests were performed with these animals before this date. B The neonatally-exposed rats were subjected subsequently to the MB test on PD27-28, to the EPM test on PD33-34, to the MB test on PD63-64 and to the EPM test on PD70-71. C The neonatally-exposed rats were subjected subsequently to the LDB test on PD16-17 and on PD30-31
The time spent in the opened arms in the EPM apparatus by PD33-34, PD70-71 and PD113-114 rats pre-exposed on PD2 to saline (SAL), dexamethasone (DEX), hypoxia (N) or dexamethasone and hypoxia (DEX×N). Data are presented as the means ± SEM. *p < 0.05 vs SAL group of the same age
The levels of marble burying activity in the MB assay demonstrated by PD27-28 and PD63-64 rats pre-exposed on PD2 to saline (SAL), dexamethasone (DEX), hypoxia (N) or dexamethasone and hypoxia (DEX×N). Data are presented as the means ± SEM. *p < 0.05 vs SAL group of the same age. #p < 0.05 vs SAL group of PD63-64 age
The time spent in the light compartment in the LDB apparatus by PD16-17 and PD30-31 rats pre-exposed on PD2 to saline (SAL), dexamethasone (DEX), hypoxia (N) or dexamethasone and hypoxia (DEX×N). Data are presented as the means ± SEM. #p < 0.1 vs SAL group of PD30-31 age
Depicted as a decision theory payoff matrix, the possible life tracks of PD2 rat pups (marked with white or yellow colour) born by mothers, which tended to have the “anxious” lifestyle with preference to dark and hypoxic underground places and limited digging (upper plates), or the “carefree” lifestyle with preference to lit and normoxic open-space places and intensive digging (lower plates) in the predator-free (left plates) or in the predator-rich habitats (right plates). Please note the fate of the yellow rat pup that was nursed by the “carefree” mother in the predator-rich environment
In mammals, a persistent increase in anxiety affects animal’s behavioral activities in adulthood consistently and might be “programmed” by early-life adverse events permanently. The “programming” of anxiety in adult subjects by severe neonatal events like cerebral hypoxia-ischemia or prolonged maternal separation is well established. By contrast, the age of onset of anxiety-related behavioral changes triggered by neonatal events of marginal intensity such as mild anoxia or a short-term exposure to glucocorticoids remains elusive to date. Here we studied anxiety-driven behaviors demonstrated in the elevated plus maze (EPM), in the marble burying (MB) and in the light–dark box (LDB) tests in adolescent and adult rats pre-exposed to an acute anoxic event and/or a single injection of synthetic glucocorticoid dexamethasone on postnatal day 2. Adult rats pre-exposed neonatally to hypoxia and dexamethasone demonstrated decreased activities either in the EPM or in the MB tests. Both exposures influenced anxiety-related activities as independent factors of similar strength, with additive impact on behaviors. In adolescent animals, the earliest behavioral changes detected after neonatal exposure to anoxia and glucocorticoids were found in the MB test at the age of one month. The findings evidenced that neonatal events of marginal intensity are capable of triggering a subsequent persistent increase in anxiety-driven behaviours in mammals, which might be detected in the adolescent age already. The identified within-generation early-life «programming» of mammalian anxiety by stress hormones and hypoxia might be considered as a possible product of prolonged predator-driven evolution and depicted like a signal-detection-theory payoff matrix. Graphic Abstract
a Map of Lake Tanganyika with sampling localities along of the investigated cichlid species (edited on http://www.simplemappr.net and Photoshop v. 13.0). Shape in black and white indicates the cichlid species which were free of monogeneans, and the groups that were included for the morphological identification only. Photos by Van Steenberge, Konings and Gessl. b anchor with the nine digitized landmarks (LM1–LM9) following Rodríguez-González et al. (2015). c Morphometric characters of the Male Copulatory Organ (MCO) of C. nshomboi parasitizing Perissodus microlepis sampled from Nyaruhongoka (NB2), with: TL total straight length; PE copulatory tube curved length; HE heel straight length and AP accessory piece straight length (Color figure online)
Geomorphometric analyses on the DA dataset of C. nshomboi specimens parasitizing boulengerochromine and perissodine hosts. Scatter plot showing the variation in shape of DA along PC1 and PC2 (a), and PC1 and PC3 (b). Wireframe graphs illustrating the shape changes from overall mean next to each PC, with starting shapes (consensus) in black and target shapes (changes + 0.1) in grey. Results from PCA and multivariate regression of PC1 (d) and PC3 (e) against log centroid size (CS) (c). The shape changes along PC1 (r = − 0.341, p ˂ 0.0001) and PC3 (r = − 0.044, p ˂ 0.0058) were correlated with anchor size. Scatter plot showing the variation in shape along CV1 and CV2 (e). Wireframe graphs illustrating the shape changes from the overall mean based on CVA are next to each PC, with starting shapes (consensus) in black and target shapes (changes + 0.7) in grey (Color figure online)
Projection of Neighbour‐Joining tree (NJ) generated from the morphometric Mahalanobis distance matrix (a) and distribution of log centroid sizes (CS) of DA (purple) and VA (orange) of C. nshomboi parasitizing against the host populations (b). The bootstrap values are indicated above the nodes for DA (in bold) and VA dataset for the groups of C. nshomboi (Color figure online)
Geomorphometric analyses on the VA dataset of C. nshomboi specimens parasitizing boulengerochromine and perissodine hosts. Scatter plot showing the variation in shape of VA along PC1 and PC2 (a), and PC1 and PC3 (b). Wireframe graphs illustrating the shape changes from overall mean based on PCA are next to each PC, with starting shapes (consensus) in black and target shapes (changes + 0.1) in grey. Results from PCA and multivariate regression of PC1 (d) and PC3 (e) against log centroid size (CS) (c). The shape changes along PC1 (r = − 0.3121, p ˂ 0.0001) and PC3 (r =  − 0.1382, p ˂ 0.0001) were correlated with anchor size. Scatter plot showing the variation in shape along CV1 and CV2 (e). Wireframe graphs illustrating the shape changes from overall mean based on CVA are next to each PC, with starting shapes (consensus) in black and target shapes (changes + 0.7) in grey (Color figure online)
Procrustes distance matrix (left of the diagonal) obtained from DA (in bold) and VA dataset among the studied populations of C. nshomboi based on nine LMs, with p-values from permutation test with 10,000 randomizations (right of the diagonal) (significant p-values after Holm–Bonferroni correction are indicated by ‘*’)
As hosts constitute the resource for parasites, an adaptive radiation in a host can drive one in a parasite. In Lake Tanganyika, the diversification of cichlids has often led to a diversification of their Cichlidogyrus monogeneans. Hitherto, Cichlidogyrus nshomboi was known only from Boulengerochromis microlepis, the sole member of Boulengerochromini. Surprisingly, we retrieved this monogenean from Perissodus microlepis, P. straeleni and Haplotaxodon microlepis, belonging to Perissodini. We sequenced the nuclear 18S, 28S, ITS1 rDNA, and the mitochondrial COI genes and studied the morphology of the male copulatory organ (MCO) and the anchors of the attachment organ. This confirmed the conspecificity of the specimens. The occurrence of C. nshomboi on unrelated host lineages could be explained by inheritance from a common ancestor, or by host-switching. We further investigated the genetic and morphological variation across taxonomic (host tribes and species) and geographical scales. Results revealed divergence in ITS1 and COI between parasites infecting different tribes, which could indicate incipient speciation. Additionally, morphological differentiation in the shape and size of anchors was found between these groups, which could be attributed to phenotypic plasticity or to adaptation. Monogeneans from large-bodied B. microlepis had significantly larger anchors, whereas only two of the four measurements differed for the MCO. Unexpectedly, no morphological variation was observed between specimens infecting different species of Perissodini from nearby localities. However, differences were found between C. nshomboi infecting P. microlepis from different parts of the lake, which could be linked to the population genetic structure of the host.
To understand how adaptive divergence emerges it is essential to examine the function of phenotypic traits along a continuum. For vertebrates, the mandible provides a key link with foraging and other important activities which has made it highly relevant for investigations of biomechanical change. Variation in mandible shape is known to correspond with ecology but its function is often only investigated between distinct species. However, for such divergence to occur and be maintained selection likely draws from many sources of biomechanical variation. African cichlids represent an exemplar model for understanding how such processes unfold with mandible variation existing between species, sexes, and is likely generated in nature by the potential for hybridization. We explored such mandible variation through a finite element modelling approach and predicted that hybrids and females would have reduced functional capabilities, the former in line with disruptive selection and the latter due to potential trade-offs incurred by maternal mouthbrooding in Malawian haplochromines. We revealed evidence of structural adaptations between Tropheops 'Red Cheek' and Labeotrophues fuelleborni that impacted the dispersion of mechanical stress in ways that matched the foraging of these species. Also, hybrids showed higher stresses relative to both species across the mandible. Sexual dimorphism in stress handling was evident despite minor differences in shape with males showing enhanced load resistance. However, in hybrids it appeared that males were disadvantaged relative to females, and displayed asymmetry in load handling. Together, these results show evidence of species and sex based biomechanical variation, that could be targeted by divergent selection.
Key components of the notochord signaling system, part of a proposed BpIM. In the transverse section of axial structures shown here, inductive interactions across embryonic tissues are influenced primarily by dorsoventral gradients of signaling molecules Shh, BMP, and Wnt
A simplified illustration of the SPN showing the basic positive feedback circuit, its implementation in forming parasegmental boundaries, and the phase shift of parasegments and segments. The segmented germband stage has been identified as an arthropod “phylotypic stage” (shown here in Drosophila)
A body plan is a stable configuration of characters for a major taxonomic group, such as chordates or arthropods. Despite widespread casual reliance on the concept for guiding comparisons within and between groups, the nature of body plans as well as the biological causes underlying their evolution have remained elusive. This paper proposes an abstract mechanistic model of body plan identity. We hypothesize that body plans are an evolutionary phenomenon that only applies to a relatively small subset of major clades, rather than being associated with each and every so-called “phylum.” Body plans arise in evolution by stepwise accretion, and require a level of developmental complexity that is only found in some animal clades. Further, we suggest that, parallel to the developmental mechanisms controlling character identity, there are “body plan identity mechanisms” (BpIMs) that maintain entire configurations of characters while possessing a mechanistic architecture that is itself stable and traceable through evolutionary change. These BpIMs, we suggest, are entrenched intercellular signaling networks operating between transient embryonic structures that are destined to differentiate into distinct individualized characters. The activity of a BpIM results in a transient long-range integration of the embryo that is highly sensitive to genetic and environmental perturbations, and that can be detected morphologically as a conserved phylotypic stage. This model is illustrated with detailed interpretations of the notochord signaling system and the segment polarity network as candidate BpIMs in vertebrates and arthropods, respectively. We conclude by contrasting the proposed developmental-mechanistic conception of body plans with the phylogenetic notion of ground plans, and sketch the general outlines of an empirical research program on body plan evolution.
The variation in residual brain size (green) and maximum longevity in log transformed (purple) in 26 families (shown in the y axis) from both Anura and Urodela orders. Black line—mean, box—SE, whiskers—1.96*SE. Sample sizes in parentheses are shown at the right vertical axis
The variation in relative brain size (blue) and maximum longevity in log transformed (orange) in 34 families (shown in the y axis) representing all known reptilian orders. Black line—mean, box—SE, whiskers—1.96*SE. Sample sizes in parentheses are shown at the right vertical axis
The relationships of whole brain mass (in log transformed) with body mass (in log transformed) and lifespan (in log transformed) among reptiles (a, c) and amphibians (b, d)
The evolution of brain size is constrained by the trade-off between the energetic costs allocated towards its maintenance and the cognitive advantages that come with a larger brain, leading to a paradox. The cognitive benefits of larger brains (e.g., high behavioural flexibility) mitigate extrinsic mortality factors, which may indirectly select for slower ageing that prolongs lifespan (“cognitive buffer hypothesis”). However, substantial energetic costs imposed by the maintenance of neural tissue is expected to compromise the energetic budget of large-brained organisms, and their investment in somatic maintenance and repair, thus accelerating ageing that shortens lifespan (the “disposable soma theory”). The relationship between lifespan and brain size has mostly been investigated in birds and mammals. Thus, whether these trade-offs express across ectothermic vertebrates remains to be addressed on a large-scale. Our study presents the first large-scale analysis of the brain size-lifespan relationship in ectothermic tetrapods (amphibians and reptiles). Using a dataset spanning 265 species, we performed phylogenetic linear models to investigate the predicted trade-off between variation in brain size and longevity. Our findings revealed a negative relationship between brain size and lifespan across reptiles, whereas no association was observed across amphibians. Thus, the relationship between life history and brain evolution in ectotherms does not follow the general pattern found across other vertebrates. Among ectotherms, the high metabolic cost of producing neural tissue seems to transcend the cognitive benefits of evolving a larger brain. Consequently, our findings suggest that natural selection favours optimization of the energetic economy over the fitness-advantages that cognitive benefits may offer.
Example of the effect of two different superimposition methods on the interpretation of results. Viscosi and Cardini (2011, p. e25630): “A set of 10 random triangles (raw data) was superimposed either using Bookstein baseline superimposition (a1) or Procrustes (b1). Shape coordinates were subjected to PCAs whose results were illustrated using biplots (a2, b2) showing both the scatterplot of the specimens (filled circles) and the loadings (dotted lines) used to weight the matrix (X1, Y1, etc.) of shape coordinates. Shape variation at the positive extreme of PC1 was visualized magnified four times using either displacement vectors (a3, b3) or TPS grids (a4, b4)”
Example configuration of 2D landmarks (1–10) and semilandmarks (11–60) on the labial side of a marmot hemimandible. Semilandmarks are used to measures outline curves in between ‘fixed’ landmarks except in three regions which we describe using only landmarks: the first region without semilandmarks is the upper margin of the symphysis (between landmark 1 and 2), which is short and almost straight; the other two are the alveolar rim of the incisor and toothrow (between landmarks 1 and 10, and between landmarks 3 and 4), where the bone is thin and often damaged
Marmot hemimandibles superimposed using different methods (a–e), as explained in the main text. Abbreviations: minPRD indicates sliding using the minimum Procrustes distance criterion; minBE indicates sliding by minimizing bending energy. The hemimandibular data analysed during this study are included in this published article as supplementary information files
Bar plots showing ‘per-landmark’ variances (each landmark and semilandmark) with black and white bars for respectively the maximum and minimum values, red and yellow bars for the values being in the 10% of the respectively largest and lowest values, and grey bars for the remaining values of ‘per-landmark’ variances (dark grey for those above the median and light grey for those below)
Same type of bar plot as in Fig. 4 but now showing variance of simulated data with circular (isotropic) variation around each landmark
Landmark-based geometric morphometrics using the Procrustes approach has become the dominant family of methods in morphometrics. However, the superimposition (and sliding, if semilandmarks are present), that transforms raw coordinates into shape coordinates is biologically arbitrary. Procrustes has desirable statistical properties, but is not based on a biological model. The same is true for sliding methods. These techniques allow powerful statistical analyses of a full set of shape coordinates, but make the use of subsets of landmarks/semilandmarks problematic, inaccurate and misleading, if not totally wrong. Crucially, the biological arbitrariness of the superimposition prevents any meaningful quantification, analysis and interpretation of variation one landmark/semilandmark at a time. We exemplify how misleading this type of analyses can be by using a real dataset, as well as simulated data with isotropic variation. Both show inconsistencies in ‘per-landmark/semilandmark’ variances. The simulation in fact helps to make even more obvious that the pattern of variance is strongly influenced by the biologically arbitrary choice of the mathematical treatment. Unfortunately, despite this limitation of all superimposition methods being known since the early days of Procrustean morphometrics, there has been a recent series of papers in leading journals presenting results of ‘per-landmark’ analyses. Thus, we further clarify why these analyses are wrong and represent misleading examples that should not be followed: Procrustes shape data cannot be analyzed, visualized or interpreted one landmark at a time. For users who are in doubt, in the Conclusions, we provide a short list of recommendations on how to easily avoid this type of mistakes.
All skeletal specimens of the North American dinosaur Tyrannosaurus and a number of trace fossils have been attributed to the single species: T. rex. Although an unusual degree of variation in skeletal robustness among specimens and variability in anterior dentary tooth form have been noted, the possibility of sibling species within the genus Tyrannosaurus has never been tested in depth in both anatomical and stratigraphic terms. New analysis, based on a dataset of over three dozen specimens, finds that Tyrannosaurus specimens exhibit such a remarkable degree of proportional variations, distributed at different stratigraphic levels, that the pattern favors multiple species at least partly separated by time; ontogenetic and sexual causes being less consistent with the data. Variation in dentary incisiform counts correlate with skeletal robusticity and also appear to change over time. Based on the current evidence, three morphotypes are demonstrated, and two additional species of Tyrannosaurus are diagnosed and named. One robust species with two small incisors in each dentary appears to have been present initially, followed by two contemporaneous species (one robust and another gracile) both of which had one small incisor in each dentary, suggesting both anagenesis and cladogenesis occurred. The geological/geographic forces underlying the evolution of multiple Tyrannosaurus species are examined. A discussion of the issues involving the recognition and designation of multiple morphotypes/species within dinosaur genera is included.
Study area and the sites of fish and data collection across the Lake Kronotskoe basin
The Lake Kronotskoe kokanee genetic differentiation, feeding and spatial distribution, as well as food recourse distribution during the ice-free period. a Admixture coefficient plot for 160 samples generated in Structure for K = 2. Each individual is represented as a vertical line partitioned into coloured segments representative of an individual's fractional membership in the given cluster. Mean p-values for the clusters = 0.92 (1, SR morph) and 0.93 (2, DR morph). b The relationship between the number of gill rakers and δ¹³C value. c The occurrence of food objects in the stomachs of the SR and DR morphs. d The ratio of the SR and DR morphs in the different zones wherein SR is given above the line and DR below. e The weighted averaged zooplankton abundance in g/m³ for each layer expressed as percentage of the sum between all layers. f The weighted averaged benthos abundance in g/m² for each layer expressed as percentage of the sum between all layers (lit littoral, sl slope, int intermediate and pf profundal zones)
Segregation of the kokanee morphs in the Lake Kronotskoe tributaries during the reproduction period and the comparison of the SR and DR morphs from two watercourses by the number of gill rakers
Early ontogeny timing and environmental conditions of development for the Lake Kronotskoe kokanee. a The temperatures throughout the annual periods at the spawning sites of the SR (orange and red) and DR (blue and green) morphs, the developmental timing for each group obtained through direct experiment is given above the graph in the same timescale. b Lakeward migration timing for the SR (orange and red) and DR (blue, teal and green) morphs, shadings demonstrate the range of II–III quarters of migration in all blocks. c The temperature conditions in the lake in the II–III quarters of lakeward run. d The dynamics of biomass in the pelagic and benthic food niches throughout the year for zooplankton (collected from the bottom to surface on the station with maximal depth) and ice-free period for benthos (slope sites with 15–40 m depth) (Color figure online)
Fish diversification into sympatric ecomorph pairs demonstrates a striking parallelism across a number of taxa in numerous lakes. However, there is a dearth of information on environmental conditions, which may orchestrate divergence processes across generations. Here we explore whether the environmental factors affecting food and reproductive niche distinctions could trigger the divergence of the lacustrine-riverine fish species into two morphs based on kokanee Oncorhynchus nerka of the Lake Kronotskoe. We reveal drastic differences in temperature on the tributary reproduction sites affecting the early ontogeny timing and disrupting the time of lakeward migration of the morphs. The juveniles of the benthivorous morph run into the lake in spring during the food abundance peak on the slope, while the planktivorous kokanee migrates to the lake in the summer when the pelagic zone abounds with zooplankton. The dynamics of this food niches is determined by water temperature dynamics and may be stable for long periods of time, thus making each morph adapting to similar condition throughout generations. We suggest that the pelagic-benthic divergence could be explained by the factors, which are extrinsic for fish, making our results applicable for numerous cases of this microevolutionary pathway all over the Holarctic.
Analysis of the developmental sequence variability provides data linking the ontogeny and phylogeny of the investigated objects. Here, we present a study of cranial ossifications sequence variability in the polyphyletic group of Cyprininae Barbus sensu lato (Cypriniformes, Teleostei). We analyzed the intra- and interspecific variability, compared sequences of closely related and phylogenetically distant species, reconstructed an alleged ancestral sequence, and assessed the sequence variations’ evolutionary validity. As the results, we revealed that the observed sequence alterations occur due to intrinsic, likely genetic or epigenetic factors. The skull ossifications, as well as skull regions, differ in the variability level. The ossifications appearing at the intermediate phase and skull regions composing splanchnocranium are most variable. In contrast, the structures emerging at the early and late phases of skull development and regions of neurocranium are less variable. The majority of sequence alterations are non-adaptive and selectively neutral. Increase in their number accompanying the transition from intra- to interspecific and intergeneric levels resembles the accumulation of the selectively neutral genetic variations accompanying the increase of phylogenetic distance. Reconstructions of phylogenetic relationships between investigated species obtained with the analyses of sequence similarity and phylogenetic analyses using parsimony (PAUP) are consistent with the phylogenies based on molecular data and thus demonstrate the potential of sequence analysis for phylogenetic inference.
The operational harmony between living beings and their circumstances, their ever-changing environment, is a constitutive condition of their existence. Nutrition and symbiosis are two essential aspects of this harmony. Disruption of the symbiosis between host and gut microbiota, the so-called dysbiosis, as well as the inadequate diet from which it results, contribute to the etiology of immunometabolic disorders. Research into the development of these diseases is highly influenced by our understanding of the evolutionary roots of metabolic functioning, thereby considering that chronic non-communicable diseases arise from an evolutionary mismatch. However, the lens has been mostly directed toward energy availability and metabolism, but away from our closest environmental factor, the gut microbiota. Thus, this paper proposes a narrative thread that places symbiosis in an evolutionary perspective, expanding the traditional framework of humans’ adaptation to their food environment.
Connectivity patterns of the hindlimb in aquatic birds. A Schematic representation of the anatomical elements involved in the analysis. Bones (or ossified cartilages or tendons) and links between bones are indicated in yellow and muscles and links through muscles are indicted in orange. B–I Networks of different aquatic birds. Colors of the silhouettes indicate the locomotor habit (black = ND; blue = LFPD; green = HFPD; red = WPD). BAechmophorus, CAlca torda, DAnas platyrhynchos, EAnhinga anhinga, FAptenodytes patagonicus, GGavia immer, HNumida meleagris, IPhalacrocorax brasilianus. A pelvis, B femur, C patella, D tibiotarsus, E fibula, F tarsometarsus, G cartilago tibialis, H os metatarsale I, I1-2 phalanges of digit I, J1-3 phalanges of digit II, K1-4 phalanges of digit III, L1-5 phalanges of digit IV, 1—IC, 2—ILPR, 3—ILPO, 4—ITCr + ITM, 5—ITC, 6—IFE, 7—IFI, 8—ISF, 9—CFC, 10—A, 11—FTI, 12—FTL, 13—FTM, 14—PO, 15—PIFL, 16—PIFM, 17—FCM, 18—FCL, 19—IF, 20—G, 21—TC, 22—FB, 23—EDL, 24—PL, 25—FDL + FHL, 26—FPPD2, 27—FPPD3, 28—FPPD4, 29—FL + FPD2 + FPD3. Muscle abbreviations are listed in Online Resources 2 and 3
Heatmap of the different AnNA parameters obtained for aquatic birds. Parameters were standardized (SD) in order to have comparable variance. ad average degree, acc average cluster coefficient, apl average path length, d density, e links, h heterogeneity, HFPD highly foot-propelled divers, LFPD lesser foot-propelled divers, n nodes, nd network diameter, ND non-divers, p parcellation, WPD wing-propelled divers
Phylomorphospace of PCA values on aquatic bird species from the time-calibrated phylogeny of Prum et al. (2015). Contribution to each component is indicated in pink in the right lower corner. ad average degree, acc average cluster coefficient, apl average path length, d density, e links, h heterogeneity, HFPD highly foot-propelled divers, LFPD lesser foot-propelled divers, n nodes, nd network diameter, ND non-divers, p parcellation, WPD wing-propelled divers
To study the hindlimb connectivity patterns of aquatic birds, we compared the musculoskeletal multi-networks of non-divers (Numididae and Anatidae), wing-propelled divers (Alcidae and Sphenicidae), and foot-propelled divers (Anhingidae, Phalacrocoracidae, Podicipedidae, and Gaviidae). Anatomical multi-networks are undirected multigraphs where bones and muscles were considered as nodes and the physical junctions between them as links. From each network we calculated different parameters, performed a principal component analysis and constructed a phylomorphospace. Our results show that both phylogenetic history and locomotor habits contributed to shape the musculoskeletal hindlimb connectivity of aquatic birds. Wing-propelled divers have complex and dense networks and are separated from the rest of birds, with penguins tightly clustered together. Non-divers and foot-propelled divers have loose networks and are clustered together, except for Podicipedidae and Gaviidae that are clustered together but separated from the rest. We also compared the networks of extant and fossil diving taxa and observed that complete muscular reconstructions can be compared with extant taxa, which is useful in order to include paleontological information in analyses of musculoskeletal disparity. These results encourage the exploration of the musculoskeletal connectivity patterns in other locomotor modules and taxa of different habits, in order to explore the relative contribution of ecology and phylogeny in the evolution of the connectivity of the musculoskeletal system, and to asses some generalities about the connectivity of musculoskeletal system in highly specialized taxa.
Lateral view of the right innominate bone of the pelvis and visualization of the eight pelvic trait measurements (1–8) as described in Kohn and Atchley (1988). A detailed description of each linear measurement is given in Table 2. Points represent the approximate location to place the caliper jaws when taking measurements for each linear distance. Point fill indicates the method of measurement used: open = calipers expanded to the greatest interior distance; filled = calipers retracted to the greatest exterior distance. Line style indicates visibility of the measurement plane viewed in this projection: solid = no obstruction; dashed = obscured
The four-species chronogram used in this study, pruned from the dated molecular phylogeny by Steppan and Schenk (2017). Branch lengths are scaled to millions of years ago (MYA), and the age of each ancestral node and basal contrast is displayed. Comparison pairs between G-matrices are shown as double ended arrow lines, and its inclusion within a set of comparisons is indicated by the color: All-nodes = blue, red, and white; Contrasts = blue and white; Tip-species = red and white (Color figure online)
The angle of g-max divergence among A correlation, or B covariance G-matrices against the time since divergence in millions of years. Dashed regression lines indicate non-significant slopes. Each regression set and the associated points (a comparison pair) are indicated by line color and point fill: Contrasts = blue and white; Tip-species = red and white (Color figure online)
Random skewers deviation between the A correlation, or B covariance G-matrices against the time since divergence in millions of years. Dashed regression lines indicate non-significant slopes. Each regression set and the associated points (a comparison pair) are indicated by line color and point fill: Contrasts = blue and white; Tip-species = red and white (Color figure online)
A Disparity between correlation G-matrices against the time since divergence in millions of years. B Euclidean distances among the conditional evolvabilities of each species regressed against time since divergence. Dashed regression lines indicate non-significant slopes. Each regression set and the associated points (a comparison pair) are indicated by line color and point fill: Contrasts = blue and white; Tip-species = red and white (Color figure online)
Quantitative genetics is a powerful tool for predicting phenotypic evolution on a microevolutionary scale. This predictive power primarily comes from the Lande equation (Δz̅ = Gβ), a multivariate expansion of the breeder’s equation, where phenotypic change (Δz̅) is predicted from the genetic covariances (G) and selection (β). Typically restricted to generational change, evolutionary biologists have proposed that quantitative genetics could bridge micro- and macroevolutionary patterns if predictions were expanded to longer timescales. While mathematically possible, making quantitative genetic predictions across generations or species is contentiously debated, principally in assuming long-term stability of the G-matrix. Here we tested stability at a macroevolutionary timescale by conducting full- and half-sib breeding programs in two species of sigmodontine rodents from South America, the leaf-eared mice Phyllotis vaccarum and P. darwini and estimated the G-matrices for eight pelvic traits. To expand our phylogenetic breadth, we incorporated two additional G-matrices measured for the same traits from Kohn & Atchley’s 1988 study of the murine rodents Mus musculus and Rattus norvegicus. Using a phylogenetic comparative framework and four separate metrics of matrix divergence or similarity, we found no significant association between evolutionary divergence among species G-matrices and time, supporting the assumption of stability for at least some structures. However, the phylogenetic sample size is necessarily small. We suggest that small fluctuations in covariance structure can occur rapidly, but underlying developmental regulation prevents significant divergence at macroevolutionary scales, analogous to an Ornstein–Uhlenbeck pattern. Expanded taxonomic sampling will be needed to test this suggestion.
False discovery rates of the ES-sim-GLM function in multiple regression modelling. False discovery rates were calculated as the proportion of datasets for which ES-sim-GLM incorrectly identifies trait-dependent diversification for two significance levels (0.05 and 0.1). Each pair of points represents one of the 9 simulated datasets of the liolaemids-based simulations on the Liolaemidae tree (Esquerré et al., 2019). Each scenario refers to a unique simulated diversification scenario without trait-dependence. The 9 datasets represent different trait evolution settings. (i) ‘1cladefixed’: Brownian motion with one randomly selected clade (> 10% of the total number of tips) fixed for a single trait value from one of its tips; (ii) ‘1cladenosignal’: Brownian motion overall but with one randomly selected clade lacking phylogenetic signal; (iii) ‘BM’: Brownian motion; (iv) ‘BMjump’: Brownian motion with a jump in the mean values in one random clade; (v) ‘BMmultirate’: Brownian motion with one rate shift in a randomly selected clade; (vi) ‘discretetrait’: one shift between two discrete trait distributions; (vii) ‘nosignal’: no phylogenetic signal in the trait; (viii) ‘OUstrong’: Ornstein–Uhlenbeck process with a single optimum and "strong" pull; (ix) ‘OUweak’: Ornstein–Uhlenbeck process with a single optimum and “weak” pull
Performance of two tests of trait-dependent diversification based on simulations with complete phylogenies in single and multiple regression modelling. Methods are compared under different models relating speciation rates and trait values. Intensity refers to the slope used in the simulations of the datasets. The two methods are: ES-sim (based on Pearson’s correlation) and ES-sim-GLM (Generalized Linear Model). We used four different tree sizes: 50, 100, 250, and 1250 species
From left to right: phylogeny of Liolaemidae lizards (n = 216) with the genera name highlighted for simplicity, inverse of the equal-splits metric of speciation rates obtained from the full phylogeny (λ258), snout-to-vent length metric (SVL) and geographic range size metric (Range). Phylogeny is from Esquerré et al. (2019)
Identifying the role of quantitative variables on speciation rates is among the main purposes of trait-dependent diversification methods. ES-sim, a recent simulation-based approach that relies on Pearson’s correlations, allows testing trait-dependent diversification for single regression models. Here, we modified this approach to include generalized linear models and two independent variables. To examine the effects of multiple traits on speciation we modified ES-sim and integrated generalized linear models instead of Pearson’s correlations. We named the new approach as ES-sim-GLM. We further evaluated how this modified method performs in both single and multiple regression modelling. For this, we analyzed the relationship of speciation rates with geographic range size and snout-to-vent length in 216 species from the family Liolaemidae, a South American radiation of Andean lizards. Based on simulations, ES-sim-GLM for single regression models shows high power, low false discovery rates and is robust to incomplete taxon sampling. ES-sim-GLM for multiple regression models shows lower power but also low false-discovery rates. Both remained computationally efficient. Using Liolaemidae data, we found that larger species but with smaller species geographic range sizes were associated with higher speciation rates. To the best of our knowledge, no study as addressed these relationships in this clade. Our results provide new insights on macroevolutionary methods that should be relevant to all organisms and facilitate future studies that aim to understand diversification patterns across the Tree of Life.
Fourier series are usually employed to describe closed or open, 2D or 3D outlines of biological samples. Landmark-based morphometric methods are widely used in the analysis of 3D surfaces. There are few investigations on the representation and morphometric analysis of 3D biological sample surfaces with methods relating to Fourier series. In this paper, we firstly extend discrete cosine transform (DCT), a Fourier-related method classically used to describe 2D open curves, but here to 3D surfaces. Surfaces are transformed into 3D curves with a path connecting all points. The path can be determined manually by an analyst or by algorithms. Before being represented with DCT, non-shape effects should be eliminated. A strategy to improve the selection of coefficients to approximate surfaces is also presented. As a result, the mathematical homology of the coefficients is preserved while fast convergence of the approximation is ensured. Three 3D surface examples are transformed into 3D curves and represented with DCT. The first example is four groups of 120 simulated surfaces generated with equations, and the other two examples are 3D surfaces extracted from aligned 3D human skulls with four types of diagnoses of coronal craniosynostosis. Principal component analysis, one-way analysis of similarity, and one-way permutational multivariate analysis of variance are utilized to analyze the coefficients obtained. The results of statistical analyses suggest that DCT is an effective and stable tool in describing 3D surfaces.
The breast-shoulder apparatus (BSA) poses a particular challenge for morphological comparisons, since its skeletal components display a great degree of mobility with respect to one another. We employed computed tomography to visualise the skeletal elements of the BSA of Anolis lizards from the Greater Antillean islands, and use four different methods to compare its structural morphology: geometric morphometric analysis of (a) isolated elements of the BSA, (b) a common shape space projection, (c) the BSA in situ, adherent to a standardised configuration, and (d) qualitative-descriptive comparison. Our findings of morphological variability of the BSA relate directly to functional-morphological demands imposed by the microhabitat specialisation of these lizards. Surprisingly, the combination of the mobile elements of the BSA into one in situ structure did not reveal a greater disparity between groups than the analysis of the moieties in isolation. However, examining this structure in situ added spatial information that could not be examined with previous approaches. Trunk-ground anoles are characterised by the relative anteroposterior extent of the presternum, interclavicle, and coracoid, likely impacting the muscle vectors and power output of humeral pro- and retractors, and emphasising humeral adduction in trunk-ground anoles. Shape differences that indicate a trajectory from trunk-crown, to crown-giant, to twig anoles are continuous. These consist of complementary shape variation in all skeletal elements of the BSA and describe a relatively lateromedially narrower BSA and an anteroposteriorly shorter epicoracoid towards twig forms, without altering the direction of the major muscle vectors in this region.
Modeling approach and phylogenetic context. A Network model of the human skull. Nodes represent bones and links represent physical joints (sutures and synchondroses). Topological variables help us to measure the structure and organization of network models. Their actual meaning depends on the nature of the relations that are being modelled as links (Butts, 2009). In skull networks links represent sutures and synchondroses, which embody growth and functional relations among bones (Herring & Teng, 2000; Opperman, 2000; Rafferty et al., 2003; Di Ieva et al., 2013), therefore, topological variables translate into morphological features that depend on growth and function, such as integration, modularity, and disparity (see Box 1). The six topological variables used here are illustrated with colors. D is the number of links (in gray) given the maximum number of links possible, which depends on the total number of nodes. C is the number of 3-node loops given the maximum number of loops possible (in blue, the 3-node loop between temporal, parietal, and occipital). L is the mean of all shortest paths (in green, shortest path of length two between the left maxilla and temporal). P is the even partition of nodes into many modules (dashed red lines indicate the three modules identified using an optimization algorithm, see Methods). H is the heterogeneity of connections among nodes and A is the correlation of connectivities: note how bones vary in their connections (the black circle size within nodes is proportional to their number of connections relative to the most connected node, the ethmoid with 13); in yellow, the connections of the four links of the lacrimal and of the 12 links of the sphenoid illustrate the two extremes of the variation. B Evolutionary relations of sampled mammals. The skulls of primates (including representatives of the Strepsirrhini and Haplorhini suborders) was compared with a diverse set of mammals spanning 12 orders, including marsupials and monotremes (Color figure online)
Phylomorphospace of skull network models defined by the two rotated components. Primates and non-primates occupy different regions of the space, with primates having larger values of RC1 and RC2 meaning that they have more anatomically integrated skulls and a greater disparity among bones than the other non-primate mammals sampled. Interestingly, the bat Pteropus directly occupies a position within the space occupied by primates (dashed line circle). The fact that bats share with primates a pervasive pattern of bone fusions during development may explain having a similar degree of anatomical disparity and disparity among bones
PGLS fits of brain size on anatomical integration. The baseline model (dashed black line) fitted the data better than the alternative models where primates (in green) and non-primates (in blue) have different slope and/or intercept. Note that the fit represented by the blue like is not significant and it has been included only for comparison and to show the alternative models compared (Color figure online)
The primate skull hosts a unique combination of anatomical features among mammals, such as a short face, wide orbits, and big braincase. Together with a trend to fuse bones in late development, these features define the anatomical organization of the skull of primates—which bones articulate to each other and the pattern this creates. Here, I quantified the anatomical organization of the skull of 17 primates and 15 non-primate mammals using anatomical network analysis to assess how the skulls of primates have diverged from those of other mammals, and whether their anatomical differences coevolved with brain size. Results show that primates have a greater anatomical integration of their skulls and a greater disparity among bones than other non-primate mammals. Brain size seems to contribute in part to this difference, but its true effect could not be conclusively proven. This supports the hypothesis that primates have a distinct anatomical organization of the skull, but whether this is related to their larger brains remains an open question.
Phylogenetic relationship among Liolaemus lizards based on molecular sequences. Species belonging to Argentinean group-blue; species belonging to Chilean group-red. Right panel indicates presence/absence of precloacal pores in males and females (colour figure online).
Evolution of the mode of male precloacal pores showing: A Best fitted model, i.e., meristic model where transitions rates (q) occur in a stepwise fashion in both directions, showing that some character states transition higher than others (higher = red, medium = violet and low = blue); B Ancestral states reconstruction where pie diagrams at each node represent ancestral states more likely on these and the colour branch the posterior probability of character occurrence based on mean from 1000 simulations (colour figure online).
Ancestral state reconstruction using hidden rates model. Pie diagrams at each node represent ancestral states on these following two rate categories R1-slower and R2-faster. Note that the evolutionary rate of female precloacal evolution is not uniform among the species included in the analysis. Those species belonging to Argentinean group Eulaemus have in general faster rates (except by L. boulengeri group and L. lineomaculatus section), while those species belong to Chilean group has slower rates. Left rectangle shows the different rate categories (R) and states based on mode of precloacal pores
Positive association between male phylogenetic residuals of the snout volume and A Precipitation; B Log10 solar radiation and C Temperature. Species belonging to Argentinean group-blue; species belonging to Chilean group-red (colour figure online).
Negative association between the male phylogenetic residuals of the eye surface and: A Precipitation; B Log10 solar radiation and C Wind speed. Species belonging to Argentinean group-blue; species belonging to Chilean group-red (colour figure online).
Animals obtain environmental information using different sensory modalities, and sensory organ size allows inferences concerning the importance of these modalities, which depend on numerous evolutionary or ecological factors. Here, we test whether sex, different evolutionary processes and climatic factors explain chemical and visual sensory organ size in South American Liolaemus lizards as a model. We obtained snout volume (vomeronasal organ proxy), eye surface area, and counted the number of secretory precloacal pores in males and females of 61 species. For evolutionary processes, we tested phylogenetic signal, and different evolutionary models; as well as compared evolutionary rate changes on these traits. We also explored different climatic factors associated with changes in these traits. Our results showed the majority of studied traits had low phylogenetic signal and fit a variety of models. Number of precloacal pores showed greater phylogenetic signal in both sexes and best fit a model of evolution with differential rate transitions model, and have a more complex evolution in females versus males. In males, snout volume correlated positively with precipitation, solar radiation and temperature; while male eye surface area was negatively associated with precipitation, solar radiation and wind speed. However, females appear to be more influenced by intrinsic evolutionary processes whereas males were more influenced by climatic factors. This is the first study exploring the evolution of female precloacal pores in squamates reptiles in general and provides evidence that sex and sensory modality type are strong predictive factors of sensory organ size.
An example of Gylt PCR products after digestion by Eco47 III. Labels at the bottom of the gel represent uncleaved homozygotes (U), cleaved homozygotes (C) and heterozygous genotypes respectively
Proportions of fishes with genotypes conforming to one of six possible classes of parental or hybrid genotypes with a scaled likelihood > 0.5 according to a NewHybrids (Anderson & Thompson, 2002) analysis. F.h and F.g respectively represent Fundulus heteroclitus and F. grandis parental genotypes. F1 and F2 denote first and second-generation hybrids while BXh and BXg represent backcrosses to F. heteroclitus and F. grandis respectively
The frequency of fishes collected for different 5 mm size classes in each of the three collection years
Frequencies of alleles typical of Fundulus grandis (g) at four loci for fishes of different size (age) classes collected in each of the three years of the study. Black bars represent the larger of the two size classes while grey bars identify the smaller of the two size classes. These collections encompass two cohorts, the small fishes collected in 2015 and the large fishes of 2016 representing cohort one, and the small fishes collected in 2016 and the large fishes from 2017 representing cohort two (identified by horizontal bars at the top of the figure). The numbers at the bottom of each bar show the number of individuals in the sample
Genotype frequencies of three nuclear loci for two different cohorts of killifish. Panel A shows cohort 1 (small size of 2015 in grey, large size of 2016 in black) while panel B shows cohort 2 (small size of 2016 in grey, large size of 2017 in black). Alleles typical of F. heteroclitus are denoted with “h” while alleles of F. grandis are “g.”
Hybrid zones provide excellent opportunities to study speciation processes and ecological interactions between recently diverged taxa. Historically, hybrid zones have been divided into those in which fitness of hybrids is independent of the environment, and those in which environmental factors influence the fitness of different genotypes. The present study investigated the temporal genetic patterns at a location within a hybrid zone between the killifish Fundulus heteroclitus and F. grandis, in an effort to determine the extent and directionality of hybridization and the fitness of different genotypes. Fishes collected over the course of three years were placed into two age classes and genotyped at three nuclear loci and one mitochondrial locus that are highly differentiated between the species, allowing for comparison of genetic patterns between different age classes of the same cohorts. Individuals of hybrid descent were prevalent at the study site, the majority of which were likely advanced generation hybrids or backcrosses to one of the parental taxa. The cohort analyses revealed decreased abundance of both single and dilocus hybrid genotypes, and directional changes in allele frequency with increased age in some, but not all cohorts. These fluctuating patterns of selection across the course of the study suggest that fitness is likely strongly influenced by environmental factors.
The accurate determination of the spatial trends on the variability of a species' gene pool is essential to elucidate the underlying demographic-evolutionary events, thus helping to unravel the microevolutionary history of the population under study. Herein we present a new software called GenoCline, mainly addressed to detect genetic clines from allele, haplotype, and genome-wide data. This program package allows identifying the geographic orientation of clinal genetic variation through a system of iterative rotation of a virtual coordinate axis. Besides, GenoCline can perform complementary analyses to explore the potential origin of the genetic clines observed, including spatial autocorrelation, isolation by distance, centroid method, multidimensional scaling and Sammon projection. Among the advantages of this software is the ease in data entry and potential interconnection with other programs. Genetic and geographic data can be entered in spreadsheet table formatting (.xls), whereas genome-wide data can be imported in Eigensoft format. Genetic frequencies can also be exported in a format compatible with other programs dealing with population genetic and evolutionary biology analyses. All illustrations of results are saved in .svg format so that there will be high quality and easily editable vectorial graphs available for the researcher. Being implemented in Java, GenoCline is highly portable, thus working in different operating systems.
The recently described 890-million-year-old sponge fossil illuminates the early evolutionary path to the emergence of animal sentience. A sentient animal is aware of feelings and sensations due to the activity of a nervous system. Indirect markers suggest that the foundations of sentience originated hundreds of millions of years before the Cambrian. If the first neuron was a sensory cell, the presence of epithelial “neural stem cells” in ancient Porifera may have been the ancestral state of the nerve cell that appeared in Eumetazoa. In addition, sponges have neurotransmitters, such as Glutamate and GABA, and other molecular markers, such as EflMsiA, Piezo ion channel and Notch. If the 890-million-year-old fossil is identified as a sponge, the emergence of the buiding blocks of sentience among animals began much earlier than previously thought.
Several papers have recently raised the occurrence of some problems with between-group Principal Component Analysis (bgPCA). This method inflates the differences between the groups, and can even display completely artificial differences when none exist, for example when applied to random numbers tables with many variables (columns) and few individuals (rows). Lately, cross-validation has been proposed as a way to circumvent this problem. Here we present some tools and several functions of the ade4 package for the R statistical software to compute a bgPCA, test the presence of statistically significant groups, perform a cross-validation of this analysis and compute associated statistics. We also describe how to use these functions to avoid running into the spurious groups problem. Several examples, including a real data set and random numbers tables, are used to validate this approach in various experimental and numerical conditions. The integrated framework of the duality diagram, as implemented in ade4, allows to extend this approach to other multivariate analysis methods beyond principal component analysis, which could prove useful in the case of other types of variables. The R code and the real data table used to make the computations and graphs of this paper are available as supplementary material.
A matrix manipulation new to the quantitative study of develomental stability reveals unexpected morphometric patterns in a classic data set of landmark-based calvarial growth. There are implications for evolutionary studies. Among organismal biology’s fundamental postulates is the assumption that most aspects of any higher animal’s growth trajectories are dynamically stable, resilient against the types of small but functionally pertinent transient perturbations that may have originated in genotype, morphogenesis, or ecophenotypy. We need an operationalization of this axiom for landmark data sets arising from longitudinal data designs. The present paper introduces a multivariate approach toward that goal: a method for identification and interpretation of patterns of dynamical stability in longitudinally collected landmark data. The new method is based in an application of eigenanalysis unfamiliar to most organismal biologists: analysis of a covariance matrix of Boas coordinates (Procrustes coordinates without the size standardization) against their changes over time. These eigenanalyses may yield complex eigenvalues and eigenvectors (terms involving $$i=\sqrt{-1}$$ i = - 1 ); the paper carefully explains how these are to be scattered, gridded, and interpreted by their real and imaginary canonical vectors. For the Vilmann neurocranial octagons, the classic morphometric data set used as the running example here, there result new empirical findings that offer a pattern analysis of the ways perturbations of growth are attenuated or otherwise modified over the course of developmental time. The main finding, dominance of a generalized version of dynamical stability (negative autoregressions, as announced by the negative real parts of their eigenvalues, often combined with shearing and rotation in a helpful canonical plane), is surprising in its strength and consistency. A closing discussion explores some implications of this novel pattern analysis of growth regulation. It differs in many respects from the usual way covariance matrices are wielded in geometric morphometrics, differences relevant to a variety of study designs for comparisons of development across species.
A Posterior oblique view of thoracolumbar vertebrae of individual 4.081. Syndesmophytes and costovertebral joint fusion. Image courtesy of Wim van Est. B, C Anterior (B) and lateral (C) views of thoracolumbar vertebrae of individual 2.427. Marginal syndesmophytes (arrowheads) fused the vertebral column into a “bamboo spine.” Isolated calcification of longitudinal ligaments (curved arrows) is present at the upper-most lumbar vertebra and from lumbar six to the sacrum. There is wedge-shaped collapse of the sixth lumbar vertebra and fusion with the seventh, associated with reactive new bone formation and apparent draining sinuses (straight arrows). Images courtesy of Wim van Est
Lateral view of lumbar vertebrae of individual 3.158. Marginal (arrow) and non-marginal (arrowheads) syndesmophytes. Images courtesy of Wim van Est
Anterior view of human thoracic vertebrae. Syndesmophytes bridging produces image of a bamboo spine. Costovertebral joint fusion is also noted
This review identifies the character of inflammatory arthritis in the Baboon Catacomb mummies, notes change in prevalence of the disease over the millennia and provides insight to ancient Egyptian animal husbandry. Examination was performed on (1) 80 Papio anubus from the Baboon Catacomb, (2) a group of twentieth century free-ranging baboons from Ethiopia, Kenya and Tanzania and (3) human skeletons from sympatric, synchronic Egyptian cemeteries. Spondyloarthropathy is recognized in Papio (baboons) on the basis of syndesmophytes, zygapophyseal joint fusion, appendicular joint subchondral erosions and reactive new bone formation. Vitamin D deficiency is recognized by bowed bones and angulation of epiphyseal-diaphyseal junctions; infection spondylitis, by draining sinuses and reactive new bone formation. Fulfillment of the above listed diagnostic criteria support the diagnosis of spondyloarthropathy in 6% of Catacomb baboons, indistinguishable in prevalence from the 3.8% in twentieth century Papio anubus and 2.3–4.4% of sympatric, synchronic Egyptian humans. Evidence of vitamin D deficiency was present in three-fifths of afflicted baboons. The prevalence of spondyloarthropathy remains indistinguishable across time and phylogeny (human and baboon), suggesting that the hygienic conditions under which the baboons were housed are equal to that of synchronic human inhabitants.
Evolutionary trends (ETs) are traditionally defined as substantial changes in the state of traits through time produced by a persistent condition of directional evolution. ETs might also include directional responses to ecological, climatic or biological gradients and represent the primary evolutionary pattern at high taxonomic levels and over long-time scales. The absence of a well-supported operative definition of ETs blurred the definition of conceptual differences between ETs and other key concepts in evolution such as convergence, parallel evolution, and divergence. Also, it prevented the formulation of modern guidelines for studying ETs and evolutionary dynamics related to them. In phenotypic evolution, the theory of morphodynamics states that the interplay between evolutionary factors such as phylogeny, evo-devo constraints, environment, and biological function determines morphological evolution. After introducing a new operative definition, here we provide a morphodynamics-based framework for studying phenotypic ETs, discussing how understanding the impact of these factors on ETs improves the explanation of links between biological patterns and processes underpinning directional evolution. We envisage that adopting a quantitative, pattern-based, and multifactorial approach will pave the way to new potential applications for this field of evolutionary biology. In this framework, by exploiting the catalysing effect of climate change on evolution, research on ETs induced by global change might represent an ideal arena for validating hypotheses about the predictability of evolution.
The area under investigation and the spawning sites location (a), spawning timeframe (b), as well as positions of the spawning sites and the characteristics of confluences in the Unana River basin (c). The labels demonstrate the centre of the allocated spawning sections (areas) and the height of spawning for each of seven morphs (labeled with letters, the spawning site and timeframe for the 8th N1a-morph is not known)
T3 muscle content in adult individuals of the Lake Kronotskoe morphs (labeled with letters) in midsummer. Mean values (line) ± SE (boxes) and Min–Max values (whiskers) are shown
Within the sympatric evolution framework a range of ecological variables are considered as potential initiators and controllers of the diversification process. Here, we identify the proximate factors providing the reproductive isolation among seven sympatric ecomorphs of the genus Salvelinus charr dwelling in the Lake Kronotskoe basin (North-East Asia). We demonstrate that the slope profile of the lake tributaries determining the water flow velocity and position of the groundwater discharges serves as a barrier between the reproductive sites of the ecomorphs and provides the basis for selective pressure affecting the Lake Kronotskoe fish during spawning. The main characteristic under selection is a migratory ability, which is determined by the swimming performance and the amount of energy reserved in the body and depends on fish morphology and physiology. The flex points indicating abrupt slope changes along the spawning watercourse restrict the upstream migration of the groups having a comparatively low swimming performance and energy reserve. A thorough analysis of the ecomorphs’ migratory and spawning activity indicated two energy expenditure strategies: the fish could invest most of the energy either on migration or spawning. Our findings supported with data on fish ecology, morphology, and thyroid hormone status allow us to put forward a following hypothesis. We suggest that the interplay of spatially heterogeneous environmental variables affecting life history decisions via ecomorphological and physiological traits could serve as a trigger for the reproductive isolation among the ecomorphs in a single ecosystem.
Evolutionary invasion analysis seeks to identify those phenotypes that cannot be invaded and replaced by alternative organismal strategies. This is achieved by first constructing a dynamical system that governs a rare mutant’s dynamics when introduced into an ecological setting at equilibrium with a resident strategy. From this, a mutant fitness function is derived whose analysis is dependent on the complexity of the ecological milieu. Invasion analyses of age-, stage-, space-, or otherwise-structured populations typically require that a fitness function, termed the invasion fitness, be extracted as an eigenvalue of the linearized dynamics of the focal organism’s ecology. This poses little technical difficulty when populations are structured into a small number (usually < 4) of compartments. However, for more complex ecologies, calculating the invasion fitness can be difficult. Here we present an algorithm to perform such analyses in class-structured populations, even when the resulting dimensionality is high enough to prohibit the direct calculation of a dominant eigenvalue. This algorithm also allows for an assessment of the evolutionary stability and convergence stability conditions, thus providing a tool for the complete evolutionary analysis of class-structured populations.
Relationship between A mean seed size and environmental seasonality and B within-plant variation in seed size and environmental unpredictability for nine populations of D. scandens. Seasonality and unpredictability are defined as the seasonal and the residual variance components of mean-scaled monthly precipitation, where mean scaling is achieved by dividing by the grand mean squared. The
Illustration of D. scandens blossom inflorescence and trait measurements. The depicted blossom is in the first day of the bisexual phase with the first male flower open. The resin-producing gland is visible above the male flowers and the three stigmas of the three female flowers are below the cluster of male flowers. The measurement illustrated on the right are: GHr and GHl for gland height right and left, and SWr, SWc, SWl for stigma width, right, centre, and left.
(Photo C. Pélabon, drawings M. Carlson)
Relationship between trait mean and within-blossom variation for A seed size, B gland height and C stigma width. The within blossom variation in seed size is measured by the standard deviation SD in seed diameter, and the within-blossom variation for the two other traits is measured by their fluctuating asymmetry. Grey dots represent individual blossom measurements, black dots represent population means. Black lines represent the regressions of the within-blossom variation on the blossom mean for each population. These regressions are presented when statistically supported and parameter estimates are obtained from models fitted on data expressed on the original scale (mm)
Relationship between A mean seed size and environmental seasonality and B within-plant variation in seed size and environmental unpredictability for nine populations of D. scandens. Seasonality and unpredictability are defined as the seasonal and the residual variance components of mean-scaled monthly precipitation, where mean scaling is achieved by dividing by the grand mean squared. The models for the weighted regressions are for A: mean seed size = 3.79 (± 0.18) + 0.63 (± 0.50) × seasonality, and for B: 100 × standard deviation of seed size = 8.62 (± 3.31) + 21.78 (± 12.65) × unpredictability. Note that the imprecision of both environmental characteristics may generate attenuation of the regression slope particularly for environmental unpredictability. SD standard deviation
Within-plant variation in seed size may merely reflect developmental instability, or it may be adaptive in facilitating diversifying bet-hedging, that is, production of phenotypically diverse offspring when future environments are unpredictable. To test the latter hypothesis, we analyzed patterns of variation in seed size in 11 populations of the perennial vine Dalechampia scandens grown in a common greenhouse environment. We tested whether population differences in the mean and variation of seed size covaried with environmental predictability at two different timescales. We also tested whether within-plant variation in seed size was correlated with independent measures of floral developmental instability and increased under stressful conditions. Populations differed genetically in the amount of seed-size variation occurring among plants, among infructescences within plants, and among seeds within infructescences. Within-individual variation was not detectably correlated with measures of developmental instability and did not increase under stress, but it increased weakly with short-term environmental unpredictability of precipitation at the source-population site. These results support the hypothesis that greater variation in seed size is adaptive when environmental predictability is low.
Several studies of arboreal anuran species show morphological specializations for clinging onto narrow substrates. However, little is known about these capacities in non-specialized anurans, which is crucial to understand the initial phases of adaptation to a new niche. To assess the functional requirements related to the evolution of arboreality in anurans we analyzed climbing performance, and correlated anatomical traits, in the terrestrial toad Rhinella arenarum, a species choose as a proxy for the ancestral condition regarding the evolution of this specialized niche. We studied the impact of a substrate of wooden rods with different diameters, arrangements, and slopes on locomotion, grasping, and climbing with a comparative framework. Animals were confronted with climbing tests, video recording their behaviors. Preserved specimens were dissected to assess limb myology, osteology, and tendons’ characteristics. Our results show that how terrestrial toad R. arenarum climbs is different from those displayed by specialized tree frogs. Animals flexed their fingers and toes, grasping the substrate displaying hookings and partial graspings. The palm was scarcely involved in the grip, as in specialized anurans. These actions were performed although flexor and extensor muscles of the digits are highly conserved and generalized. Further, we formally assess the evolutionary history of ecological and anatomical traits related to climbing among Rhinella species to improving the comprehension of the relation between morphofunctional patterns and behavioral climbing skills. Our experiments revealed that this terrestrial toad possesses unexpected climbing capacities, suggesting a way in which evolution of new niches could have developed in the evolution of anurans.
The pelvis plays an active role in weight bearing and countering the ground reaction forces incurred by the hindlimbs thus making it a critical component of the locomotor skeleton. Accordingly, this anatomical region is theoretically ideal for inferring locomotor behavior from both external skeletal morphology and trabecular microarchitecture, with the latter possibly offering nuanced insights into the mechanical loading environment given its increased plasticity and higher turnover rate. However, trabecular microarchitecture is also known to be influenced by a variety of factors including body size, sex, age, genetic regulation, diet and activity level, that collectively hinder the ability to generate consistent functional inferences. In this study, a comparative sample of mammals (42 species spanning four orders) of varying sizes, yet comparable locomotor repertoires, were evaluated to determine the effects of body size, phylogeny and locomotion on hipbone trabecular microarchitecture. This study found a weak functional signal detected in differences in bone volume fraction and the degree of anisotropy across certain pre-assigned locomotor categories, while confirming previously recognized allometric scaling trends reported for other mammalian samples based on the femur. Within primates, a more anisotropic pattern was observed for quadrupedal species attributed to their repetitive loading regimes and stereotypical limb excursions, while isotropic values were revealed for taxa utilizing more varied arboreal repertoires. Humans, despite a frequent and predictable loading environment associated with their use of bipedalism, showed relatively isotropic values. This study highlights the confounding factors that influence trabecular microarchitecture and consequently limit its utility as a method for investigating locomotor adaptation.
Mean longevity (± SE, in days) of Drosophila buzzatii for S and C lines at each of two temperatures, 25 °C and 30 °C. Longevity is also shown for flies in a cyclic thermal regimen. Asterisks indicate significant differences (*P < 0.05)
Survival curves are shown for S and C lines of Drosophila buzzatii at 25 °C, 30 °C and a cyclic thermal environment in this study. Each curve was averaged on three replicated lines
Early fecundity (one-week mean fecundity ± SE) and two-week fecundity of females at 25 °C and 30 °C is shown for S and C lines of Drosophila buzzatii under either a constant exposure of males (CEM) or a limited exposure of males (LEM). Significant differences are indicated by an asterisk (*P < 0.05)
Adaptation to environmental temperature depends on both direct and correlated responses to selection for reproduction and survival at elevated temperature. Sexual selection is one of the most powerful of all evolutionary forces and we tested both fecundity and longevity for their correlated responses to sexual selection on the ability to mate (mating success) at high temperature. Replicated lines selected for 15 generations of mating at 33 °C (S lines) were compared to their respective controls (C lines) in D. buzzatii in three thermal regimes: 25 °C, 30 °C and a cyclic thermal regime for longevity from 17 to 32 °C. Previous work showed that S lines successfully responded for the trait selected and the present results show a trade-off in males between mating success at elevated temperature and longevity in all three thermal regimes tested. In addition, inter-sexual relationships of trade-offs were apparent between male longevity and female fecundity as correlated selection responses. In this sex-specific association of trade off, S females exhibited higher fecundity than C females at 30 °C only if females were exposed to a limited social environment of a single male. Overall, selection for mating at high temperature increases female fecundity at high temperature but decreases longevity in males. This sex-specific and negative impact on longevity in males could be the result of a genetic correlation between mating success at high temperature and reduced longevity in this sex.
Schematic diagram of two-phase testicular descent in mammals. In the first or trans-abdominal phase, the testis descends from the urogenital ridge to the inguinal region by regulating hormonal and mechanical elements. In the second or inguino-scrotal phase, testicular descent is induced from the inguinal region to the scrotum
Rapidly evolving and positively selected genes in the DHH signaling pathway in ascrotal laurasiatherians. A Five unique rapidly evolving DHH signaling pathway genes in ascrotal laurasiatherians. B Protein DHH and DHH signaling pathway in mammals. The rapidly evolving genes in ascrotal laurasiatherians are marked with a red star, while the positively selected genes in combined ascrotal laurasiatherians are marked with a green star. The left panel shows that, in the absence of the molecule DHH, Ptc blocks the function Smo, and subsequently leads to the proteolytic processing of full-length form Gli (GliFL) to repressor form Gli (GliR), which turns off the DHH signaling pathway and represses downstream target genes. The right panel illustrates that when DHH is present, it binds to Ptc and alleviates the inhibition to Smo; then GliA is released from Kif7 and the Sufu complex, resulting in the activation of downstream target genes
Positively selected DHH signaling pathway genes in laurasiatherians. Phenotype of testicular position in representative laurasiatherians in this study labeled in a well-accepted phylogeny from TimeTree (http://www.timetree.prg). Scrotal laurasiatherians are marked with an orange square, whereas ascrotal laurasiatherians are marked with a blue square. Positively selected DHH signaling pathway genes in each branch were marked by different colored bars
Specific AA substitutions in DHH signaling pathway genes in ascrotal laurasiatherians. A Specific substitutions shared in different groups of ascrotal laurasiatherians. B Specific substitutions in the protein DHH for each group of ascrotal laurasiatherians. C Specific substitutions in the protein MEGF8 for each group of ascrotal laurasiatherians
Unsuccessful descent of testes in humans and other scrotal mammals can result in cryptorchidism, consequent abnormalities and a high risk of malignancy. However, many male adult mammals possessing natural ascrotal testes are as viable and healthy as other scrotal mammals. This study performed an evolutionary analysis on the desert hedgehog (DHH) signaling pathway, an important regulator for testicular development, mainly in laurasiatherians. Significant positive selection, accelerated evolutionary rates, and specific amino acid substitutions were identified in ascrotal species, some of which caused radical changes in physicochemical and biological properties. Considering that most signs of positive selection were identified in genes responsible for or related to negative regulation, we suggest that the enhanced negative regulation of the DHH signaling pathway drives, at least in part, the evolution of ascrotal testes in laurasiatherians and other mammals. This study could provide some novel insights into the evolution of natural healthy ‘cryptorchidism’ in mammals and into the convergent molecular evolution of the complex trait.
A: Map of Ecuador showing the locations of studied sites colored red at each elevation. B: Study species. C: A species of wasp visiting female Croton flowers. D: A bee visiting male Croton flowers
Variation of morphological traits of Croton according to elevation. A: Leaf thickness increased according to specific leaf area and was higher in the High Elevation. B: Number of inflorescences increased according to plant volume and was higher in the High Elevation. C: Average inflorescence length increased according to plant volume and was higher in the Low Elevation
The regularized discriminant analysis differentiated the elevations with the climate variables studied. The first axis (PC1 explained 93% of the variance) clearly separated the three elevations while the second axis (PC2 explained 7% of the variance) clearly separated the Low Elevation from the Medium Elevation and the High Elevation that were like each other in this axis
Reciprocal crosses between elevations to determine reproductive isolation (RI) by fruit and seed set of Croton. The mean and the confidence intervals indicated reproductive isolation between Low Elevation plants and High Elevation plants according to fruit set
Fruit and seed set by treatment within each elevation. We compared differences among the four pollination treatments using a non-parametric paired Wilcoxon test after an analysis of variance. Fruit and seed set with open pollination were higher at Low Elevation compared to the other two elevations and treatments. Fruit and seed set was marginally different between within crosses and open bag treatment at High Elevation
Elevation gradients generate different environmental conditions. This environmental differentiation can influence morphological adaptation, habitat isolation, reproductive isolation, and pollinator limitation in plants. Habitat differentiation and isolation often act first on phenotypic traits and then on genotype variation, causing genetic divergences between populations. We evaluated the effect of elevation on morphological traits, reproductive isolation, and pollinator limitation in Croton aff. wagneri in dry shrublands of inter-Andean valleys in Ecuador. We measured morphological traits of Croton at three elevations and carried out experimental pollination crosses between and within each population at different elevations to assess the degree of reproductive isolation and pollinator limitation. Morphological traits such as leaf thickness, plant volume, inflorescence length and inflorescence number were dissimilar between plants in different elevations. There was evidence of incipient reproductive isolation between plants in populations at the highest and the lowest studied elevations. Pollination experiments within each elevation showed a limitation of pollinators in Croton in the highest elevation. Intrinsic barriers to pollen dispersal and ecological divergence can produce reproductive incompatibilities between individuals with different traits along the Croton elevation gradient.
Distribution of range sizes of the studied clades. Original data (in km²) were log10-transformed. Ectotherm and endotherm taxon names are indicated in blue and red, respectively. Red vertical bars correspond to the means of each distribution. Colors are used to facilitate the comparison across plots. Color palette was obtained using the viridis package (Garnier, 2018). For comparison, the solid, dashed, and dotted gray lines on the last plot indicate the areas of Europe, South America, and Africa, respectively (Color figure online)
Changes in geographical distributions underlie a variety of fundamental ecological and evolutionary processes, from allopatric speciation to local extinction. However, little is known about general principles governing the evolution of range sizes at macroevolutionary scales. In this study we measure rates of geographical range size and position in a large-scale dataset of nearly 20,000 species including mammals, birds, squamates and anurans to test three predictions regarding the relationship between endothermy and geographical range evolution, namely whether endotherms show (1) larger geographical ranges; (2) faster rates of range size evolution; and (3) faster changes in the geographical position of their ranges. We found evidence in favor of all of these predictions, suggesting that the evolution of endothermy was associated with a fundamental change in the tempo of range evolution in terrestrial vertebrates. These results are consistent with two previously hypothesized relationships between range size and metabolic rate: the thermal plasticity hypothesis, which suggests that high metabolic rate increases thermal tolerance, and the energy constraint hypothesis, which posits that due to the higher, sustained levels of energy requirements, individuals with high metabolic rates would necessitate to forage farther and to space themselves more broadly, which would result in lower population densities, larger home ranges and ultimately larger range sizes. On the other hand, there was substantial variation in rates of range size evolution among the studied taxa that cannot be explained by the evolution of endothermy alone.
The effect of large Amazonian rivers as barriers to distribution of species and gene flow has been the subject of debate for more than a century. The Madeira River is the largest tributary of the Amazon River, with the region comprising its basin undergoing complex changes from the Pliocene through the Holocene. Accordingly, the evolution of its drainage seems to have been an important factor in the biological diversification of different taxa. We characterize the phylogeographic pattern of Adelphobates quinquevittatus, focusing on the role of the Madeira River and the environmental changes in the region, as potential barriers to gene flow. For this, we used sequences of two mitochondrial genes from 65 individuals sampled in 15 locations. We identify population structure partially related to the current Madeira River configuration. However the most upstream session does not represent a historical barrier, suggesting that may have attained its current geomorphological configuration recently. Divergence among clades began in the last 1 million years, coinciding with documented changes in this landscape, and may be related to river dynamics associated with the presence of open vegetation areas. This phylogeographic pattern supports the dynamism of the drainage, and the historical complexity of the upper Madeira River.
A mass tree based on the hemagglutinin protein of 52 type B human influenza strains of the Victoria lineage displaying mutations at the numbered branch nodes
A mass tree based on the hemagglutinin protein of 60 type B human influenza strains of the Yamagata lineage displaying mutations at the numbered branch nodes
Pairwise sequence alignment of the HA0 hemagglutinin protein of the B/Hong Kong/548/2000 (denoted HK00) (UniProtKB: Q80A60) and B/Victoria/504/2000 (denoted Vic00) (UniProtKB: A5HSU7) strains showing the tryptic peptide segments (boxed) at which mutations were identified by the MassTree algorithm. The unidentified N14K mutation and position of the signal peptide cleavage site at residue R17 are marked
Map of mutations identified by the MassTree algorithm for strains of the Victoria and Yamagata lineage over the two decade period from 1996 to 2016. Numbering is according to HA0 sequences comprising 566 residues and the N-terminal signal peptide. Mutations shown in bold are common to both lineages. Those underlined occur at common locations in each lineage including reversions marked by “R” in superscript.
A mass spectrometry based phylonumerics approach has been applied to study the molecular evolution of influenza hemagglutinin of type B strains of the Victoria and Yamagata lineage. The results demonstrate that, despite the similar evolutionary topologies, the mutation profiles and diversity associated with the evolution of each lineage is very different. Most mutations occur exclusively in one lineage versus the other, and the mutation locations are largely difference. Despite this, the evolutionary dynamics share features with each other and type A hemagglutinin in that a large number of mutations in both lineages occur within known antigenic loop domains, where consecutive potential epistatic mutations occur in different loop regions, or successively within and outside such a region. The results are largely in accord with other conventional phylogenetic studies of the evolution and antigenic dynamics of such strains thus further validating the method.
Correlation structure among variables in each missing data mechanism. Circles represent model components and their intersection represents correlations among them. Blue, orange and green circles represent missing data, phylogenetic information and missing data probability, respectively. Then, in a, traits have phylogenetic signal and their values are missing randomly. In b, phylogenetic information explains missing data probability of the traits. In c, phylogenetic information is not able to explain all missing data probability
Median of the percentage of estimation error (p) for Blomberg’s K under different imputation methods, OU’s α, missing data percentage and mechanisms for simulated data. Species’ traits were deleted at random (MCAR), phylogenetically correlated (MAR-PHYLO) or correlated to an auxiliary trait without phylogenetic signal (MAR-TRAIT)
Median of the p for Moran’s I under different imputation methods, OU’s α, missing data percentage and mechanisms for simulated data. Species’ traits were deleted at random (MCAR), phylogenetically correlated (MAR-PHYLO) or correlated to a auxiliary trait without phylogenetic signal (MAR-TRAIT)
Scatterplot of imputation errors (NRMSE) and the absolute of the p for (a) Blomberg’s K and (b) Moran’s I based on the simulated data
Given the prevalence of missing data on species’ traits – the Raunkiaeran shortfall-, several methods have been proposed to fill sparse databases. However, analyses based on these imputed databases can introduce several biases. Here, we evaluated potential estimation biases caused by the use of imputed databases. In the evaluation, we considered the estimation of descriptive statistics, regression coefficient, and phylogenetic signal for different missing and imputing scenarios. We found that percentage of missing data, missing mechanisms and imputation methods were important in determining estimation errors. Imputation errors are not linearly related to estimate errors. Adding phylogenetic information provides better estimates of the evaluated statistics, but this information should be combined with other variables such as traits correlated to the missing data variable. Using an empirical dataset, we found that even traits that are strongly correlated to each other, such as brain and body size of primates, can produce biases when estimating phylogenetic signal from missing data datasets. We advise researchers to share both their raw and imputed data as well as to consider the pattern of missing data to evaluate methods that perform better for their goals. In addition, the performance of imputation methods should be mainly based on statistical estimates instead of only in imputation error.
An accurate classification is the basis for research in biology. Morphometrics and morphospecies play an important role in modern taxonomy, with geometric morphometrics increasingly applied as a favourite analytical tool. Yet, really large samples are seldom available for modern species and even less common in palaeontology, where morphospecies are often identified, described and compared using just one or a very few specimens. The impact of sampling error and how large a sample must be to mitigate the inaccuracy are important questions for morphometrics and taxonomy. Using more than 4000 crania of adult mammals and taxa representing each of the four placental superorders, we assess the impacts of sampling error on estimates of species means, variances and covariances in Procrustes shape data using resampling experiments. In each group of closely related species (mostly congeneric), we found that a species can be identified fairly accurately even when means are based on relatively small samples, although errors are frequent with fewer specimens and primates more prone to inaccuracies. A precise reconstruction of similarity relationships, in contrast, sometimes requires very large samples (> 100), but this varies widely depending on the study group. Medium-sized samples are necessary to accurately estimate standard errors of mean shapes or intraspecific variance covariance structure, but in this case minimum sample sizes are broadly similar across all groups (≈ 20–50 individuals). Overall, thus, the minimum sample sized required for a study varies across taxa and depends on what is being assessed, but about 25–40 specimens (for each sex, if a species is sexually dimorphic) may be on average an adequate and attainable minimum sample size for estimating the most commonly used shape parameters. As expected, the best predictor of the effects of sampling error is the ratio of between- to within-species variation: the larger the ratio, the smaller the sample size needed to obtain the same level of accuracy. Even though ours is the largest study to date of the uncertainties in estimates of means, variances and covariances in geometric morphometrics, and despite its generally high congruence with previous analyses, we feel it would be premature to generalize. Clearly, there is no a priori answer for what minimum sample size is required for a particular study and no universal recipe to control for sampling error. Exploratory analyses using resampling experiments are thus desirable, easy to perform and yield powerful preliminary clues about the effect of sampling on parameter estimates in comparative studies of morphospecies, and in a variety of other morphometric applications in biology and medicine. Morphospecies descriptions are indeed a small piece of provisional evidence in a much more complex evolutionary puzzle. However, they are crucial in palaeontology, and provide important complimentary evidence in modern integrative taxonomy. Thus, if taxonomy provides the bricks for accurate research in biology, understanding the robustness of these bricks is the first fundamental step to build scientific knowledge on sound, stable and long-lasting foundations.
Linear dimensions collected from each anatomical region: caudal aspect of the basicranium; medial aspect of os coxa; lateral aspect of os coxa; dorsal aspect of scapula; ventral aspect of scapula; lateral aspect of scapula; cranial aspect of clavicle. All traits were measured from the left side. Refer to Table 1 for trait descriptions. Trait measurements are demonstrated on a macaque specimen and are homologous for colobines
The scapula shares developmental and functional relationships with traits of the basicranium, vertebral column, humerus, and clavicle. As a limb girdle, it also shares analogous characteristics with the pelvis. Despite these relationships, studies of primate shoulder evolution often focus on traits of the scapula in isolation. Such analyses may lead to spurious conclusions, as they implicitly model the scapula as evolving independent of other anatomical regions. Traits of the shoulder girdle share genetic covariances with each other, as well as potential covariances with dimensions of other skeletal elements. To create accurate models of shoulder evolution, it is imperative to account for the constraints imposed by these sources of covariance. Here, we use evolutionary quantitative methods to test a model in which shoulder morphological evolution is influenced by its developmental and functional covariances with the basicranium in the Colobus genus. This evolutionary relationship is also assessed with morphology of the pelvis to provide context to the evolutionary covariance among traits of the basicranium and shoulder girdle. Our results indicate potential evolutionary implications arising from covariances among the basicranium, shoulder, and pelvis. We further propose that the shoulder and basicranium may be examples of developmental, functional, and genetic covariances among traits that manifest an evolutionary suite of mutually constrained morphologies. We demonstrate novel evolutionary relationships among the shoulder girdle and basicranium that affect not only models of primate shoulder evolution but have broader implications for modeling trait evolution across the skeleton.
The geometric morphometric (GMM) construction of Procrustes shape coordinates from a data set of homologous landmark configurations puts exact algebraic constraints on position, orientation, and geometric scale. While position as digitized is not ordinarily a biologically meaningful quantity, and orientation is relevant mainly when some organismal function interacts with a Cartesian positional gradient such as horizontality, size per se is a crucially important biometric concept, especially in contexts like growth, biomechanics, or bioenergetics. “Normalizing” or “standardizing” size (usually by dividing the square root of the summed squared distances from the centroid out of all the Cartesian coordinates specimen by specimen), while associated with the elegant symmetries of the Mardia–Dryden distribution in shape space, nevertheless can substantially impeach the validity of any organismal inferences that ensue. This paper adapts two variants of standard morphometric least-squares, principal components and uniform strains, to circumvent size standardization while still accommodating an analytic toolkit for studies of differential growth that supports landmark-by-landmark graphics and thin-plate splines. Standardization of position and orientation but not size yields the coordinates Franz Boas first discussed in 1905. In studies of growth, a first principal component of these coordinates often appears to involve most landmarks shifting almost directly away from their centroid, hence the proposed model’s name, “centric allometry.” There is also a joint standardization of shear and dilation resulting in a variant of standard GMM’s “nonaffine shape coordinates” where scale information is subsumed in the affine term. Studies of growth allometry should go better in the Boas system than in the Procrustes shape space that is the current conventional workbench for GMM analyses. I demonstrate two examples of this revised approach (one developmental, one phylogenetic) that retrieve all the findings of a conventional shape-space-based approach while focusing much more closely on the phenomenon of allometric growth per se. A three-part Appendix provides an overview of the algebra, highlighting both similarities to the Procrustes approach and contrasts with it.
I used linear and nonlinear regression to re-examine the allometric relationship between length of the cephalic horn and width of the pronotum (a measure of body size) for males of 28 species of rhinoceros beetle (Coleoptera, Scarabaeidae, Dynastinae). An earlier investigation reported that variation in relative size of the horn conforms in most of the 28 species to a pattern of discontinuous, loglinear allometry, which implies, in turn, that two different power equations are needed to describe the full range in untransformed data. My analyses indicate, however, that allometric variation is continuous in all 28 species and that pattern in each of the original bivariate distributions is well described by a single mathematical function. Allometric variation on the original, arithmetic scale is linear for some species; either linear or slightly sigmoidal for other species; and decidedly sigmoidal in still other species. So-called major and minor morphs merely represent the extremes in absolute and relative size for the horn on animals drawn from the same, continuous distribution. The different findings reported in the earlier investigation resulted from insidious problems introduced by logarithmic transformation of the original bivariate data coupled with an overly complex statistical protocol for classifying individual males as either “major” or “minor.” Attempts at classification lead inevitably to oversimplification and misrepresentation of the pattern of allometric variation. Focus needs to return to describing and interpreting pattern in untransformed observations because the relationship between the original variables is the relationship of interest.
South American Canids are endemic and form a monophyletic clade supported by molecular and morphological data, with the exception of Urocyon cinereoargenteus, which is a typical North American form. South American canids occur in almost all environments in continent, and exhibit diet diversity and large size variation. Here we analyzed the skull ontogeny by applying 3D geometric morphometric techniques, in a well-represented sample of South American canids, with the aim of exploring variation in cranial size and shape as well as evolutionary patterns of such variation. The sample consisted of 1227 crania of the 11 living species of South American canids and 92 crania of Canis lupus and Vulpes vulpes, which were considered as out-groups. South American canids exhibited similar shape and diet (they are mostly omnivorous), which implies similar mechanical commitments, which are reflected in their almost uniform skulls. However, it is possible that cranial similarity is related to a shared evolutionary history with a short time of divergence. Speothos venaticus differed in its ontogenetic trajectory, with the difference being stronger between adults of this species and the remaining canids. The skull configuration is consistent with the hyper-carnivorous diet. In the case of Chrysocyon brachyurus, size plays an important role in the structure of a skull, giving rise to remarkable morphological differences from other species, although in terminal stages of its ontogeny.
Environmental scanning electron micrographs of specimens with divergent morphologies of the soil mite Rostrozetes ovulum (Oribatida: Haplozetidae) sampled in central Amazonia.
Principal Component Analysis (PCA) of morphological traits of the soil mite Rostrozetes ovulum (Oribatida: Haplozetidae) sampled in central Amazonia. Each point represents one individual, and colors represent the habitats from which individuals were sampled.
Structural Equation Model (SEM) linking environment, form and function in the soil mite Rostrozetes ovulum (Oribatida: Haplozetidae) in central Amazonia.
Geographic isolation plays a major role in biological diversification. Yet, adaptive divergence also can occur with ongoing gene flow, but the minimal spatial scale required for this is unclear. Here, we hypothesized that local gradients in soil clay and water contents respectively select for anti-adherent and hypoxia-tolerant phenotypes in soil invertebrates, thereby driving intraspecific phenotypic divergence despite unlimited, passive dispersal. We tested this idea using the parthenogenetic oribatid mite Rostrozetes ovulum, an abundant species in tropical forest soils. We obtained 40 individuals from valleys and uplands within 4 km² of rainforest in central Amazonia, and estimated soil clay and water contents for each site. Then, we experimentally assessed submersion tolerance of each individual, measured its body size, shape and structural traits, and inferred anti-adherence from the extent of debris attached to its body. We found that morphological distance was greater between than within habitats while being independent of geographic distance, which itself was unrelated to habitat. Further, using structural equation modelling, we found that clayish soils harboured mites with fewer, larger dorsal pits that were less likely to have attached debris, consistent with an anti-adherent morphology. To a lower degree, individuals from moister soils tended to survive submersion longer, likely through anaerobiosis. These patterns could reflect phenotypic plasticity, local adaptation or some combination thereof. Altogether, they suggest that environmental gradients may trigger local-scale animal diversification in soils, contributing to the exceptional biodiversity of this substrate.
Geographical distribution of Allobates sumtuosus study sampling sites (a) in northern South America (b). Black-dotted symbols indicate localities with associated morphology, acoustic and genetic data, and hollow symbols indicate localities represented only with genetic data. See Table 1 for population acronyms
Bayesian phylogenetic tree of Allobates sumtuosus populations (at left) based on the variation of a fragment of mtDNA (16S), showing the two best supported subclades; and the result of population structure analysis (BAPS) (at right), showing the clusters recovered represented by distinct colors (k = 4). Newly sequenced specimens are highlighted in bold. Asterisks represent support values of Bayesian inference between 0.9 and 1.0 (above branches) and Maximum likelihood between 80 and 100 (below branches). Branch scale is indicated in number of substitutions per site
Haplotype network (a) generated with 77 sequences of a fragment of the 16S mtDNA (179–470 base pairs) for Allobates sumtuosus and their geographic origin (b). The size of the circles in the network indicates the relative frequency of the haplotype and the color indicates the origin of the individuals corresponding to the geographic location in the sampled space (b). See Table 1 for population acronyms
Results of the correlations among each analyzed character class (genetic, morphology and acoustic) and predictor variables (environment and latitude), obtained through a Structural Equation Modeling analysis. The results of the tests for statistical significance of the correlations can be found in Table 3
Relationships between body size (snout–vent length; SVL), air temperature and latitude with the peak frequency of the advertisement call among sampled populations of Allobates sumtuosus
Geographical and environmental distances influence the divergence of characters among biological populations, especially on a macro spatial scale, making it difficult to interpret the individual contribution of these predictor variables in the process of population differentiation. Anurans are excellent models for multi-character evolutionary studies, due to their low vagility and frequent territoriality, causing certain environmental changes to result in barriers that isolate populations. Accordingly, we propose to test the correlation of environmental and geographical distances in the absence of obvious vicariant barriers with phenotypic and genotypic population characters using, as a study model, an Amazonian litter-frog (Allobates sumtuosus). Combining univariate and multivariate analyses, and Structural Equation Modeling, we tested the general hypotheses that geographical and environmental distances affect the variation in the morphometric, acoustic and genetic characters of this frog along a latitudinal gradient at a fine spatial scale. We found that the latitudinal variation was the most correlated with the variation of the studied characters, with an explanatory force always greater than 78%. Therefore, we suggest that there is a combined effect of latitude and environment on phenotypic characteristics in A. sumtuosus. These factors shape the acoustic characters of this species through pressures on body size, as confirmed by a regression analysis showing that larger body sizes resulted in lower-spectral frequency acoustic signals. This is because the climatic environmental gradient occupied by the species promotes changes in the area-volume relationship of individuals, resulting in larger body sizes towards the Equator. Although we observed a pronounced intrapopulation genetic structure, it was not associated with phenotypic variation. In summary, our study breaks down the stages of speciation for this Amazonian litter-frog, demonstrating that environmental factors lead to changes in the sexual signal due to the variation in body size.
Top-cited authors
David Owen Francis Skibinski
Robert D. Ward
  • The Commonwealth Scientific and Industrial Research Organisation
Simone Des Roches
  • University of Washington Seattle
Tyler Hether
  • University of Oregon
Luke Harmon
  • University of Idaho