Profile of a flower: How rates of morphological evolution drive floral diversification in Ericales and angiosperms

Premise

Recent studies of floral disparity in the asterid order Ericales have shown that flowers vary strongly among families and that disparity is unequally distributed between the three flower modules (perianth, androecium, gynoecium). However, it remains unknown whether these patterns are driven by heterogeneous rates of morphological evolution or other factors.

Methods

Here, we compiled a data set of 33 floral characters scored for 414 species of Ericales sampled from 346 genera and all 22 families. We conducted ancestral state reconstructions using an equal-rates Markov model for each character. We estimated rates of morphological evolution for Ericales and for a separate angiosperm-wide data set of 19 characters and 792 species, creating “rate profiles” for Ericales, angiosperms, and major angiosperm subclades. We compared morphological rates among flower modules within each data set separately and between data sets, and we compared rates among angiosperm subclades using the angiosperm data set.

Results

The androecium exhibits the highest evolutionary rates across most characters, whereas most perianth and gynoecium characters evolve more slowly in both Ericales and angiosperms. Both high and low rates of morphological evolution can result in high floral disparity in Ericales. Analyses of an angiosperm-wide floral data set reveal that this pattern appears to be conserved across most major angiosperm clades.

Conclusions

Elevated rates of morphological evolution in the androecium of Ericales may explain the higher disparity reported for this floral module. Comparing rates of morphological evolution through rate profiles proves to be a powerful tool in understanding floral evolution.     

Do different disparity proxies converge on a common signal? Insights from the cranial morphometrics and evolutionary history of Pterosauria (Diapsida: Archosauria)

Disparity, or morphological diversity, is often quantified by evolutionary biologists investigating the macroevolutionary history of clades over geological timescales. Disparity is typically quantified using proxies for morphology, such as measurements, discrete anatomical characters, or geometric morphometrics. If different proxies produce differing results, then the accurate quantification of disparity in deep time may be problematic. However, despite this, few studies have attempted to examine disparity of a single clade using multiple morphological proxies. Here, as a case study for this question, we examine the disparity of the volant Mesozoic fossil reptile clade Pterosauria, an intensively studied group that achieved substantial morphological, ecological and taxonomic diversity during their 145+ million-year evolutionary history. We characterize broadscale patterns of cranial morphological disparity for pterosaurs for the first time using landmark-based geometric morphometrics and make comparisons to calculations of pterosaur disparity based on alternative metrics. Landmark-based disparity calculations suggest that monofenestratan pterosaurs were more diverse cranially than basal non-monofenestratan pterosaurs (at least when the aberrant anurognathids are excluded), and that peak cranial disparity may have occurred in the Early Cretaceous, relatively late in pterosaur evolution. Significantly, our cranial disparity results are broadly congruent with those based on whole skeleton discrete character and limb proportion data sets, indicating that these divergent approaches document a consistent pattern of pterosaur morphological evolution. Therefore, pterosaurs provide an exemplar case demonstrating that different proxies for morphological form can converge on the same disparity signal, which is encouraging because often only one such proxy is available for extinct clades represented by fossils. Furthermore, mapping phylogeny into cranial morphospace demonstrates that pterosaur cranial morphology is significantly correlated with, and potentially constrained by, phylogenetic relationships.     

Mosaic evolution,preadaptation, and the evolution of evolvability in apes

A major goal in postsynthesis evolutionary biology has been to better understand how complex interactions between traits drive movement along and facilitate the formation of distinct evolutionary pathways. I present analyses of a character matrix sampled across the haplorrhine skeleton that revealed several modules of characters displaying distinct patterns in macroevolutionary disparity. Comparison of these patterns to those in neurological development showed that early ape evolution was characterized by an intense regime of evolutionary and developmental flexibility. Shifting and reduced constraint in apes was met with episodic bursts in phenotypic innovation that built a wide array of functional diversity over a foundation of shared developmental and anatomical structure. Shifts in modularity drove dramatic evolutionary changes across the ape body plan in two distinct ways: (1) an episode of relaxed integration early in hominoid evolution coincided with bursts in evolutionary rate across multiple character suites; (2) the formation of two new trait modules along the branch leading to chimps and humans preceded rapid and dramatic evolutionary shifts in the carpus and pelvis. Changes to the structure of evolutionary mosaicism may correspond to enhanced evolvability that has a “preadaptive” effect by catalyzing later episodes of dramatic morphological remodeling.     

IS FLORAL SPECIALIZATION AN EVOLUTIONARY DEAD‐END? POLLINATION SYSTEM TRANSITIONS IN RUELLIA (ACANTHACEAE)

Pollination systems frequently reflect adaptations to particular groups of pollinators. Such systems are indicative of evolutionary specialization and have been important in angiosperm diversification. We studied the evolution of pollination systems in the large genus Ruellia. Phylogenetic analyses, morphological ordinations, ancestral state reconstructions, and a character mapping simulation were conducted to reveal key patterns in the direction and lability of floral characters associated with pollination. We found significant floral morphological differences among species that were generally associated with different groups of floral visitors. Floral evolution has been highly labile and also directional. Some specialized systems such as hawkmoth or bat pollination are likely evolutionary dead-ends. In contrast, specialized pollination by hummingbirds is clearly not a dead-end. We found evidence for multiple reverse transitions from presumed ancestral hummingbird pollination to more derived bee or insect pollination. These repeated origins of insect pollination from hummingbird-pollinated ancestors have not evolved without historical baggage. Flowers of insect-pollinated species derived from hummingbird-pollinated ancestors are morphologically more similar to hummingbird flowers than they are to other more distantly related insect-pollinated flowers. Finally, some pollinator switches were concomitant with changes in floral morphology that are associated with those pollinators. These observations are consistent with the hypothesis that some transitions have been adaptive in the evolution of Ruellia.     

Morphological and niche divergence of pinyon pines

The environmental variables that define a species ecological niche should be associated with the evolutionary patterns present in the adaptations that resulted from living in these conditions. Thus, when comparing across species, we can expect to find an association between phylogenetically independent phenotypic characters and ecological niche evolution. Few studies have evaluated how organismal phenotypes might mirror patterns of niche evolution if these phenotypes reflect adaptations. Doing so could contribute on the understanding of the origin and maintenance of phenotypic diversity observed in nature. Here, we show the pattern of niche evolution of the pinyon pine lineage (Pinus subsection Cembroides); then, we suggest morphological adaptations possibly related to niche divergence, and finally, we test for correlation between ecological niche and morphology. We demonstrate that niche divergence is the general pattern within the clade and that it is positively correlated with adaptation.     

Molecular Phylogeny Supports Repeated Adaptation to Burrowing within Small-Eared Shrews Genus of Cryptotis (Eulipotyphla,Soricidae)

Small-eared shrews of the New World genus Cryptotis (Eulipotyphla, Soricidae) comprise at least 42 species that traditionally have been partitioned among four or more species groups based on morphological characters. The Cryptotis mexicana species group is of particular interest, because its member species inhibit a subtly graded series of forelimb adaptations that appear to correspond to locomotory behaviors that range from more ambulatory to more fossorial. Unfortunately, the evolutionary relationships both among species in the C. mexicana group and among the species groups remain unclear. To better understand the phylogeny of this group of shrews, we sequenced two mitochondrial and two nuclear genes. To help interpret the pattern and direction of morphological changes, we also generated a matrix of morphological characters focused on the evolutionarily plastic humerus. We found significant discordant between the resulting molecular and morphological trees, suggesting considerable convergence in the evolution of the humerus. Our results indicate that adaptations for increased burrowing ability evolved repeatedly within the genus Cryptotis.     

Recent Advances on Variability, Morpho-Functional Adaptations, Dental Terminology, and Evolution of Sloths

The occasion of the Xenarthra Symposium during the ICVM 9 meeting allowed us to reflect on the considerable advances in the knowledge of sloths made by the “X-community” over the past two decades, particularly in such aspects as locomotion, mastication, diet, dental terminology, intraspecific variation, sexual dimorphism, and phylogenetic relationships. These advancements have largely been made possible by the application of cladistic methodology (including DNA analyses) and the discovery of peculiar forms such as Diabolotherium, Thalassocnus, and Pseudoglyptodon in traditionally neglected areas such as the Chilean Andes and the Peruvian Pacific desert coast. Modern tree sloths exhibit an upside-down posture and suspensory locomotion, but the habits of fossil sloths are considerably more diverse and include locomotory modes such as inferred bipedality, quadrupedality, arboreality or semiarboreality, climbing, and an aquatic or semi-aquatic lifestyle in saltwater. Modern tree sloths are generalist browsers, but fossil sloths had browsing, grazing, or mixed feeding dietary habits. Discovery of two important sloth faunas in Brazil (Jacobina) and southern North America (Daytona Beach and Rancho La Brea) have permitted evaluation of the ontogenetic variation in Eremotherium laurillardi and the existence of possible sexual dimorphism in this sloth and in Paramylodon harlani. A new dental terminology applicable to a majority of clades has been developed, facilitating comparisons among taxa. An analysis wherein functional traits were plotted onto a phylogeny of sloths was used to determine patterns of evolutionary change across the clade. These analyses suggest that megatherioid sloths were primitively semiarboreal or possessed climbing adaptations, a feature retained in some members of the family Megalonychidae. Pedolateral stance in the hindfoot is shown to be convergently acquired in Mylodontidae and Megatheria (Nothrotheriidae + Megatheriidae), this feature serving as a synapomorphy of the latter clade. Digging adaptations can only be securely ascribed to scelidotheriine and mylodontine sloths, and the latter are also the only group of grazing sloths, the remainder being general browsers.     

Inferring speciation modes in a clade of Iberian chafers from rates of morphological evolution in different character systems

Background  

Studies of speciation mode based on phylogenies usually test the predicted effect on diversification patterns or on geographical distribution of closely related species. Here we outline an approach to infer the prevalent speciation mode in Iberian Hymenoplia chafers through the comparison of the evolutionary rates of morphological character systems likely to be related to sexual or ecological selection. Assuming that mitochondrial evolution is neutral and not related to measured phenotypic differences among the species, we contrast hypothetic outcomes of three speciation modes: 1) geographic isolation with subsequent random morphological divergence, resulting in overall change proportional to the mtDNA rate; 2) sexual selection on size and shape of the male intromittent organs, resulting in an evolutionary rate decoupled to that of the mtDNA; and 3) ecological segregation, reflected in character systems presumably related to ecological or biological adaptations, with rates decoupled from that of the mtDNA.     

Arboreallty and morphological evolution in ground beetles (Carabidae: Harpalinae): testing the taxon pulse model

Abstract.— One-third to two-thirds of all tropical carabids, or ground beetles, are arboreal, and evolution of arboreality has been proposed to be a dead end in this group. Many arboreal carabids have unusual morphological features that have been proposed to be adaptations for life on vegetation, including large, hemispheric eyes; an elongated prothorax; long elytra; long legs; bilobed fourth tarsomeres; adhesive setae on tarsi; and pectinate claws. However, correlations between these features and arboreality have not been rigorously tested previously. I examined the evolution of arboreality and morphological features often associated with this habitat in a phylogenetic context. The number and rates of origins and losses of arboreality in carabids in the subfamily Harpalinae were inferred with parsimony and maximum-likelihood on a variety of phylogenetic hypotheses. Correlated evolution in arboreality and morphological characters was tested with concentrated changes tests, maximum-likelihood, and independent contrasts on optimal phylogenies. There is strong evidence that both arboreality and the morphological features examined originated multiple times and can be reversed, and in no case could the hypothesis of equal rates of gains and losses be rejected. Several features are associated with arboreality: adhesive setae on the tarsi, bilobed tarsomeres, and possibly pectinate claws and an elongated prothorax. Bulgy eyes, long legs, and long elytra were not correlated with arboreality and are probably not arboreal adaptations. The evolution of arboreal carabids has not been unidirectional. These beetles have experienced multiple gains and losses of arboreality and the morphological characters commonly associated with the arboreal habitat. The evolutionary process of unidirectional character change may not be as widespread as previously thought and reversal from specialized lifestyles or habitats may be common.     

Sampling diverse characters improves phylogenies: Craniodental and postcranial characters of vertebrates often imply different trees

Morphological cladograms of vertebrates are often inferred from greater numbers of characters describing the skull and teeth than from postcranial characters. This is either because the skull is believed to yield characters with a stronger phylogenetic signal (i.e., contain less homoplasy), because morphological variation therein is more readily atomized, or because craniodental material is more widely available (particularly in the palaeontological case). An analysis of 85 vertebrate datasets published between 2000 and 2013 confirms that craniodental characters are significantly more numerous than postcranial characters, but finds no evidence that levels of homoplasy differ in the two partitions. However, a new partition test, based on tree‐to‐tree distances (as measured by the Robinson Foulds metric) rather than tree length, reveals that relationships inferred from the partitions are significantly different about one time in three, much more often than expected. Such differences may reflect divergent selective pressures in different body regions, resulting in different localized patterns of homoplasy. Most systematists attempt to sample characters broadly across body regions, but this is not always possible. We conclude that trees inferred largely from either craniodental or postcranial characters in isolation may differ significantly from those that would result from a more holistic approach. We urge the latter.     

Journeys through discrete‐character morphospace: synthesizing phylogeny,tempo, and disparity

Palaeontologists have long employed discrete categorical data to capture morphological variation in fossil species, using the resulting character–taxon matrices to measure evolutionary tempo, infer phylogenies and capture morphological disparity. However, to date these have been seen as separate approaches despite a common goal of understanding morphological evolution over deep time. Here I argue that there are clear advantages to considering these three lines of enquiry in a single space: the phylomorphospace. Conceptually these high‐dimensional spaces capture how a phylogenetic tree explores morphospace and allow us to consider important process questions around evolutionary rates, constraints, convergence and directional trends. Currently the literature contains fundamentally different approaches used to generate such spaces, with no direct comparison between them, despite the differing evolutionary histories they imply. Here I directly compare five different phylomorphospace approaches, three with direct literature equivalents and two that are novel. I use a single empirical case study of coelurosaurian theropod dinosaurs (152 taxa, 853 characters) to show that under many analyses the literature‐derived approaches tend to reflect introduced phylogenetic (rather than the intended morphological) signal. The two novel approaches, which produce limited ancestral state estimates prior to ordination, are able to minimize this phylogenetic signal and thus exhibit more realistic amounts of phylogenetic signal, rate heterogeneity, and convergent evolution.     

The macroevolutionary consequences of phenotypic integration: from development to deep time

Phenotypic integration is a pervasive characteristic of organisms. Numerous analyses have demonstrated that patterns of phenotypic integration are conserved across large clades, but that significant variation also exists. For example, heterochronic shifts related to different mammalian reproductive strategies are reflected in postcranial skeletal integration and in coordination of bone ossification. Phenotypic integration and modularity have been hypothesized to shape morphological evolution, and we extended simulations to confirm that trait integration can influence both the trajectory and magnitude of response to selection. We further demonstrate that phenotypic integration can produce both more and less disparate organisms than would be expected under random walk models by repartitioning variance in preferred directions. This effect can also be expected to favour homoplasy and convergent evolution. New empirical analyses of the carnivoran cranium show that rates of evolution, in contrast, are not strongly influenced by phenotypic integration and show little relationship to morphological disparity, suggesting that phenotypic integration may shape the direction of evolutionary change, but not necessarily the speed of it. Nonetheless, phenotypic integration is problematic for morphological clocks and should be incorporated more widely into models that seek to accurately reconstruct both trait and organismal evolution.     

Positive correlations between molecular and morphological rates of evolution

The existence of positive associations between rates of molecular and morphological evolution (calculated from branch lengths of phylogenetic trees reconstructed using molecular and morphological characters, respectively) is important to issues of neutrality in sequence evolution, phylogenetic reconstructions assuming neutrality, and evolutionary genotype-phenotype mapping. Rates correlate positively when including branches leading to extant species (tips). Excluding tips, trends are similar, but statistical significances decrease systematically. This is due to (a) lower statistical power (excluding tips reduces sample sizes), and (b) rates are solely calculated from inaccurately reconstructed character states of extinct ancestral species, and this noise decreases correlation strengths. Correlations between molecular and morphological rates of evolution increase as more morphological characters are included for phylogenetic reconstruction. Sequence lengths apparently affect correlations along similar principles. Analyses of plant phylogenies confirm those from animals: sampling biases decrease correlations between molecular and morphological rates of evolution. Results confirm that genotype and phenotype are linked, and suggest adaptive components for molecular evolution. The discussion stresses the difficulties associated with analyses and conclusions based on data deduced from phylogenetic reconstruction.     

Functional diversity of small-mammal postcrania is linked to both substrate preference and body size

Selective pressures favor morphologies that are adapted to distinct ecologies, resulting in trait partitioning among ecomorphotypes. However, the effects of these selective pressures vary across taxa, especially because morphology is also influenced by factors such as phylogeny, body size, and functional trade-offs. In this study, we examine how these factors impact functional diversification in mammals. It has been proposed that trait partitioning among mammalian ecomorphotypes is less pronounced at small body sizes due to biomechanical, energetic, and environmental factors that favor a “generalist” body plan, whereas larger taxa exhibit more substantial functional adaptations. We title this the Divergence Hypothesis (DH) because it predicts greater morphological divergence among ecomorphotypes at larger body sizes. We test DH by using phylogenetic comparative methods to examine the postcranial skeletons of 129 species of taxonomically diverse, small-to-medium-sized (<15 kg) mammals, which we categorize as either “tree-dwellers” or “ground-dwellers.” In some analyses, the morphologies of ground-dwellers and tree-dwellers suggest greater between-group differentiation at larger sizes, providing some evidence for DH. However, this trend is neither particularly strong nor supported by all analyses. Instead, a more pronounced pattern emerges that is distinct from the predictions of DH: within-group phenotypic disparity increases with body size in both ground-dwellers and tree-dwellers, driven by morphological outliers among “medium”-sized mammals. Thus, evolutionary increases in body size are more closely linked to increases in within-locomotor-group disparity than to increases in between-group disparity. We discuss biomechanical and ecological factors that may drive these evolutionary patterns, and we emphasize the significant evolutionary influences of ecology and body size on phenotypic diversity.     

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

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

Rates of phenotypic evolution of ecological characters and sexual traits during the Tanganyikan cichlid adaptive radiation

Theory suggests that sexual traits evolve faster than ecological characters. However, characteristics of a species niche may also influence evolution of sexual traits. Hence, a pending question is whether ecological characters and sexual traits present similar tempo and mode of evolution during periods of rapid ecological divergence, such as adaptive radiation. Here, we use recently developed phylogenetic comparative methods to analyse the temporal dynamics of evolution for ecological and sexual traits in Tanganyikan cichlids. Our results indicate that whereas disparity in ecological characters was concentrated early in the radiation, disparity in sexual traits remained high throughout the radiation. Thus, closely related Tanganyikan cichlids presented higher disparity in sexual traits than ecological characters. Sexual traits were also under stronger selection than ecological characters. In sum, our results suggest that ecological characters and sexual traits present distinct evolutionary patterns, and that sexual traits can evolve faster than ecological characters, even during adaptive radiation.     

Evolution of the hominoid vertebral column: The long and the short of it

The postcranial axial skeleton exhibits considerable morphological and functional diversity among living primates. Particularly striking are the derived features in hominoids that distinguish them from most other primates and mammals. In contrast to the primitive catarrhine morphotype, which presumably possessed an external (protruding) tail and emphasized more pronograde trunk posture, all living hominoids are characterized by the absence of an external tail and adaptations to orthograde trunk posture. Moreover, modern humans evolved unique vertebral features that satisfy the demands of balancing an upright torso over the hind limbs during habitual terrestrial bipedalism. Our ability to identify the evolutionary timing and understand the functional and phylogenetic significance of these fundamental changes in postcranial axial skeletal anatomy in the hominoid fossil record is key to reconstructing ancestral hominoid patterns and retracing the evolutionary pathways that led to living apes and modern humans. Here, we provide an overview of what is known about evolution of the hominoid vertebral column, focusing on the currently available anatomical evidence of three major transitions: tail loss and adaptations to orthograde posture and bipedal locomotion.     

牛科(哺乳纲:偶蹄目)动物与生境利用有关的适应形态模式

对广义牛科动物颅后骨骼的多元变量分析揭示了牛科生境利用和体型之间的骨学特征。利用逐步分辨分析方法和一个基于机器学习的决策树方法鉴别了每种生境中牛科动物颅后解剖结构的形态特征。从110个广义牛科动物测量了43个指标进行了这项分析。利用所有主要肢骨测量值和以单根肢骨测量为主的测量值获得的分辨函数和决策树可以完美地区分适应开阔生境、森林和山地的牛科动物(在所有分析中得到了100 %正确的再分类)。由于调整的函数仅涉及到很小的颅后骨骼测量集,这些函数可以应用于研究考古学和古生物学发掘物中保存的不完整标本。这些表征生境利用的生态适应函数与那些用颅齿部性状建立、用于推测牛科动物食物选择的函数结合,具有刻画已灭绝的分类类群的古个体生态学和重建古环境的潜力。我们还分析了多元回归是否较单一因子回归表现出较高的预测能力,并提出了从每一种单根主要肢骨测量的颅后形态变量得到的最好代数函数     

Extant‐only comparative methods fail to recover the disparity preserved in the bird fossil record

Most extant species are in clades with poor fossil records, and recent studies of comparative methods show they have low power to infer even highly simplified models of trait evolution without fossil data. Birds are a well‐studied radiation, yet their early evolutionary patterns are still contentious. The fossil record suggests that birds underwent a rapid ecological radiation after the end‐Cretaceous mass extinction, and several smaller, subsequent radiations. This hypothesized series of repeated radiations from fossil data is difficult to test using extant data alone. By uniting morphological and phylogenetic data on 604 extant genera of birds with morphological data on 58 species of extinct birds from 50 million years ago, the “halfway point” of avian evolution, I have been able to test how well extant‐only methods predict the diversity of fossil forms. All extant‐only methods underestimate the disparity, although the ratio of within‐ to between‐clade disparity does suggest high early rates. The failure of standard models to predict high early disparity suggests that recent radiations are obscuring deep time patterns in the evolution of birds. Metrics from different models can be used in conjunction to provide more valuable insights than simply finding the model with the highest relative fit.