Measuring changes in articulate brachiopod morphology before and after the Permian mass extinction event: do developmental constraints limit morphological innovation?

The pattern of decreasing disparity has been observed in both the metazoans and metaphytes throughout the Phanerozoic. The pattern is manifest as a decreasing trend in the origination of higher taxa. Currently, two competing evolutionary hypotheses have been proposed to explain this phenomenon: the empty ecospace hypothesis and the developmental constraint hypothesis. To empirically distinguish between these hypotheses, the change in disparity before and after the end-Permian mass extinction event was measured in the articulated brachiopods. The assumption is that ecospace-limiting constraints are removed after mass extinctions revealing the effect of developmental constraints. For each taxon within the group, both continuous and discrete character sets were analyzed. Four different measures of disparity were used to analyze each character suite. Additionally, a separate analysis was performed on a subset of the articulated brachiopods, the rhynchonellids and terebratulids. In most cases investigated, disparity rebounded to comparable levels, with the rhynchonellids and terebratulids showing the largest increase in disparity after the end-Permian extinction, a clear example of an increase in disparity without a significant increase in taxonomic diversity. The results indicate that developmental constraints may not be responsible for the decreasing disparity in this group. The more likely scenario is that increasingly structured ecological guilds have made it much more difficult for large increases in disparity to occur.     

The complex effects of mass extinctions on morphological disparity

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

DISPARITY: MORPHOLOGICAL PATTERN AND DEVELOPMENTAL CONTEXT

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

Evolution of ecospace occupancy by Mesozoic marine tetrapods

Ecology and morphology are different, and yet in comparative studies of fossil vertebrates the two are often conflated. The macroevolution of Mesozoic marine tetrapods has been explored in terms of morphological disparity, but less commonly using ecological‐functional categories. Here we use ecospace modelling to quantify ecological disparity across all Mesozoic marine tetrapods. We document the explosive radiation of marine tetrapod groups in the Triassic and their rapid attainment of high ecological disparity. Late Triassic extinctions led to a marked decline in ecological disparity, and the recovery of ecospace and ecological disparity was sluggish in the Early Jurassic. High levels of ecological disparity were again achieved by the Late Jurassic and maintained during the Cretaceous, when the ecospace became saturated by the Late Cretaceous. Sauropterygians, turtles and ichthyosauromorphs were the largest contributors to ecological disparity. Throughout the Mesozoic, we find that established groups remained ecologically conservative and did not explore occupied or vacant niches. Several parts of the ecospace remained vacant for long spans of time. Newly evolved, radiating taxa almost exclusively explored unoccupied ecospace, suggesting that abiotic releases are needed to empty niches and initiate diversification. In the balance of evolutionary drivers in Mesozoic marine tetrapods, abiotic factors were key to initiating diversification events, but biotic factors dominated the subsequent generation of ecological diversity.     

Decoupling of morphological disparity and taxic diversity during the adaptive radiation of anomodont therapsids

Adaptive radiations are central to macroevolutionary theory. Whether triggered by acquisition of new traits or ecological opportunities arising from mass extinctions, it is debated whether adaptive radiations are marked by initial expansion of taxic diversity or of morphological disparity (the range of anatomical form). If a group rediversifies following a mass extinction, it is said to have passed through a macroevolutionary bottleneck, and the loss of taxic or phylogenetic diversity may limit the amount of morphological novelty that it can subsequently generate. Anomodont therapsids, a diverse clade of Permian and Triassic herbivorous tetrapods, passed through a bottleneck during the end-Permian mass extinction. Their taxic diversity increased during the Permian, declined significantly at the Permo–Triassic boundary and rebounded during the Middle Triassic before the clade''s final extinction at the end of the Triassic. By sharp contrast, disparity declined steadily during most of anomodont history. Our results highlight three main aspects of adaptive radiations: (i) diversity and disparity are generally decoupled; (ii) models of radiations following mass extinctions may differ from those triggered by other causes (e.g. trait acquisition); and (iii) the bottleneck caused by a mass extinction means that a clade can emerge lacking its original potential for generating morphological variety.     

Reconciling molecules and morphology: molecular systematics and biogeography of Neotropical blennies (Acanthemblemaria)

Neotropical reef fish communities are species-poor compared to those of the Indo-West Pacific. An exception to that pattern is the blenny clade Chaenopsidae, one of only three rocky and coral reef fish families largely endemic to the Neotropics. Within the chaenopsids, the genus Acanthemblemaria is the most species-rich and is characterized by elaborate spinous processes on the skull. Here we construct a species tree using five nuclear markers and compare the results to those from Bayesian and parsimony phylogenetic analyses of 60 morphological characters. The sequence-based species tree conflicted with the morphological phylogenies for Acanthemblemaria, primarily due to the convergence of a suite of characters describing the distribution of spines on the head. However, we were able to resolve some of these conflicts by performing phylogenetic analyses on suites of characters not associated with head spines. By using the species tree as a guide, we used a quantitative method to identify suites of correlated morphological characters that, together, produce the distinctive skull phenotypes found in these fishes. A time calibrated phylogeny with nearly complete taxon sampling provided divergence time estimates that recovered a mid-Miocene origin for the genus, with a temporally and geographically complex pattern of speciation both before and after the closure of the Isthmus of Panama. Some sister taxa are broadly sympatric, but many occur in allopatry. The ability to infer the geography of speciation in Acanthemblemaria is complicated by extinctions, incomplete knowledge of their present geographic ranges and by wide-spread taxa that likely represent cryptic species complexes.     

Moving towards a better understanding of iterative evolution: an example from the late Silurian Monograptidae (Graptolithina) of the Baltic Basin

Iterative evolution has proved a difficult evolutionary phenomenon to study and interpret. Inferences of causality vary from study to study and quantitatively based phylogenetic reconstruction has never been attempted. In an effort to better understand iterative evolution we employed stratocladistics, gap analysis and disparity analysis to study the case of the Monograptidae in the aftermath of the late Silurian Cyrtograptus lundgreni extinction event. Our combination of gap analytical and stratocladistic techniques allowed us to elucidate the evolutionary relationships between the studied taxa. Based on our stratocladistic results we recommend the generic reassignment of five monograptid taxa. The stratocladistic results, in conjunction with morphological disparity analysis suggest the presence of a persistent developmental potential for the emergence of iteratively evolving characters. This persistent potential appears to be limited by extrinsic ecological constraints, which would have relaxed in the aftermath of the C. lundgreni extinction event. Our findings indicate that iterative evolution in the late Silurian Monograptidae is a product of the interaction of both intrinsic and extrinsic constraints on the acquisition of the iteratively evolving character, with the exact causality being dependent on the particular character.     

Self-similarity in biological classifications.

Size distributions of supraspecific taxa, e.g. genera, measured as the number of included subtaxa, e.g. species, are found to follow a power law. This behaviour has been verified for a number of taxa of different size and taxonomic rank, thus suggesting a fractal structure of biological classifications. This is regarded as probably dependent on evolutionary processes shaping the phylogenetic tree, especially speciation and extinction, as well as on the topological properties of developmental constraints and/or of the ecospace(s) with which the group has been confronted during its history. The role of taxonomic bias is deemphasized.     

Severe extinction and rapid recovery of mammals across the Cretaceous–Palaeogene boundary,and the effects of rarity on patterns of extinction and recovery

The end‐Cretaceous mass extinction ranks among the most severe extinctions of all time; however, patterns of extinction and recovery remain incompletely understood. In particular, it is unclear how severe the extinction was, how rapid the recovery was and how sampling biases might affect our understanding of these processes. To better understand terrestrial extinction and recovery and how sampling influences these patterns, we collected data on the occurrence and abundance of fossil mammals to examine mammalian diversity across the K‐Pg boundary in North America. Our data show that the extinction was more severe and the recovery more rapid than previously thought. Extinction rates are markedly higher than previously estimated: of 59 species, four survived (93% species extinction, 86% of genera). Survival is correlated with geographic range size and abundance, with widespread, common species tending to survive. This creates a sampling artefact in which rare species are both more vulnerable to extinction and less likely to be recovered, such that the fossil record is inherently biased towards the survivors. The recovery was remarkably rapid. Within 300 000 years, local diversity recovered and regional diversity rose to twice Cretaceous levels, driven by increased endemicity; morphological disparity increased above levels observed in the Cretaceous. The speed of the recovery tends to be obscured by sampling effects; faunas show increased endemicity, such that a rapid, regional increase in diversity and disparity is not seen in geographically restricted studies. Sampling biases that operate against rare taxa appear to obscure the severity of extinction and the pace of recovery across the K‐Pg boundary, and similar biases may operate during other extinction events.     

From success to persistence: Identifying an evolutionary regime shift in the diverse Paleozoic aquatic arthropod group Eurypterida,driven by the Devonian biotic crisis

Mass extinctions have altered the trajectory of evolution a number of times over the Phanerozoic. During these periods of biotic upheaval a different selective regime appears to operate, although it is still unclear whether consistent survivorship rules apply across different extinction events. We compare variations in diversity and disparity across the evolutionary history of a major Paleozoic arthropod group, the Eurypterida. Using these data, we explore the group's transition from a successful, dynamic clade to a stagnant persistent lineage, pinpointing the Devonian as the period during which this evolutionary regime shift occurred. The late Devonian biotic crisis is potentially unique among the “Big Five” mass extinctions in exhibiting a drop in speciation rates rather than an increase in extinction. Our study reveals eurypterids show depressed speciation rates throughout the Devonian but no abnormal peaks in extinction. Loss of morphospace occupation is random across all Paleozoic extinction events; however, differential origination during the Devonian results in a migration and subsequent stagnation of occupied morphospace. This shift appears linked to an ecological transition from euryhaline taxa to freshwater species with low morphological diversity alongside a decrease in endemism. These results demonstrate the importance of the Devonian biotic crisis in reshaping Paleozoic ecosystems.     

Is regional species diversity bounded or unbounded?

Two conflicting hypotheses have been proposed to explain large‐scale species diversity patterns and dynamics. The unbounded hypothesis proposes that regional diversity depends only on time and diversification rate and increases without limit. The bounded hypothesis proposes that ecological constraints place upper limits on regional diversity and that diversity is usually close to its limit. Recent evidence from the fossil record, phylogenetic analysis, biogeography, and phenotypic disparity during lineage diversification suggests that diversity is constrained by ecological processes but that it is rarely asymptotic. Niche space is often unfilled or can be more finely subdivided and still permit coexistence, and new niche space is often created before ecological limits are reached. Damped increases in diversity over time are the prevalent pattern, suggesting the need for a new ‘damped increase hypothesis'. The damped increase hypothesis predicts that diversity generally increases through time but that its rate of increase is often slowed by ecological constraints. However, slowing due to niche limitation must be distinguished from other possible mechanisms creating similar patterns. These include sampling artifacts, the inability to detect extinctions or declines in clade diversity with some methods, the distorting effects of correlated speciation‐extinction dynamics, the likelihood that opportunities for allopatric speciation will vary in space and time, and the role of undetected natural enemies in reducing host ranges and thus slowing speciation rates. The taxonomic scope of regional diversity studies must be broadened to include all ecologically similar species so that ecological constraints may be accurately inferred. The damped increase hypothesis suggests that information on evolutionary processes such as time‐for‐speciation and intrinsic diversification rates as well as ecological factors will be required to explain why regional diversity varies among times, places and taxa.     

The radiation of cynodonts and the ground plan of mammalian morphological diversity

Cynodont therapsids diversified extensively after the Permo-Triassic mass extinction event, and gave rise to mammals in the Jurassic. We use an enlarged and revised dataset of discrete skeletal characters to build a new phylogeny for all main cynodont clades from the Late Permian to the Early Jurassic, and we analyse models of morphological diversification in the group. Basal taxa and epicynodonts are paraphyletic relative to eucynodonts, and the latter are divided into cynognathians and probainognathians, with tritylodonts and mammals forming sister groups. Disparity analyses reveal a heterogeneous distribution of cynodonts in a morphospace derived from cladistic characters. Pairwise morphological distances are weakly correlated with phylogenetic distances. Comparisons of disparity by groups and through time are non-significant, especially after the data are rarefied. A disparity peak occurs in the Early/Middle Triassic, after which period the mean disparity fluctuates little. Cynognathians were characterized by high evolutionary rates and high diversity early in their history, whereas probainognathian rates were low. Community structure may have been instrumental in imposing different rates on the two clades.     

The ghosts of mammals past: biological and geographical patterns of global mammalian extinction across the Holocene

Although the recent historical period is usually treated as a temporal base-line for understanding patterns of mammal extinction, mammalian biodiversity loss has also taken place throughout the Late Quaternary. We explore the spatial, taxonomic and phylogenetic patterns of 241 mammal species extinctions known to have occurred during the Holocene up to the present day. To assess whether our understanding of mammalian threat processes has been affected by excluding these taxa, we incorporate extinct species data into analyses of the impact of body mass on extinction risk. We find that Holocene extinctions have been phylogenetically and spatially concentrated in specific taxa and geographical regions, which are often not congruent with those disproportionately at risk today. Large-bodied mammals have also been more extinction-prone in most geographical regions across the Holocene. Our data support the extinction filter hypothesis, whereby regional faunas from which susceptible species have already become extinct now appear less threatened; they may also suggest that different processes are responsible for driving past and present extinctions. We also find overall incompleteness and inter-regional biases in extinction data from the recent fossil record. Although direct use of fossil data in future projections of extinction risk is therefore not straightforward, insights into extinction processes from the Holocene record are still useful in understanding mammalian threat.     

Tooth morphology elucidates shark evolution across the end-Cretaceous mass extinction

Sharks (Selachimorpha) are iconic marine predators that have survived multiple mass extinctions over geologic time. Their prolific fossil record is represented mainly by isolated shed teeth, which provide the basis for reconstructing deep time diversity changes affecting different selachimorph clades. By contrast, corresponding shifts in shark ecology, as measured through morphological disparity, have received comparatively limited analytical attention. Here, we use a geometric morphometric approach to comprehensively examine tooth morphologies in multiple shark lineages traversing the catastrophic end-Cretaceous mass extinction—this event terminated the Mesozoic Era 66 million years ago. Our results show that selachimorphs maintained virtually static levels of dental disparity in most of their constituent clades across the Cretaceous–Paleogene interval. Nevertheless, selective extinctions did impact apex predator species characterized by triangular blade-like teeth. This is particularly evident among lamniforms, which included the dominant Cretaceous anacoracids. Conversely, other groups, such as carcharhiniforms and orectolobiforms, experienced disparity modifications, while heterodontiforms, hexanchiforms, squaliforms, squatiniforms, and †synechodontiforms were not overtly affected. Finally, while some lamniform lineages disappeared, others underwent postextinction disparity increases, especially odontaspidids, which are typified by narrow-cusped teeth adapted for feeding on fishes. Notably, this increase coincides with the early Paleogene radiation of teleosts as a possible prey source, and the geographic relocation of disparity sampling “hotspots,” perhaps indicating a regionally disjunct extinction recovery. Ultimately, our study reveals a complex morphological response to the end-Cretaceous mass extinction and highlights an event that influenced the evolution of modern sharks.

Analysis of the tooth morphology of sharks across the end-Cretaceous mass extinction, 66 million years ago, shows that while generally unaffected, some apex predator shark lineages were selectively impacted; changing habitats and the differential survival of ‘fish-eating’ sharks also reveals responses to ecological cataclysm.     

Phylogenetic Clustering of Origination and Extinction across the Late Ordovician Mass Extinction

Mass extinctions can have dramatic effects on the trajectory of life, but in some cases the effects can be relatively small even when extinction rates are high. For example, the Late Ordovician mass extinction is the second most severe in terms of the proportion of genera eliminated, yet is noted for the lack of ecological consequences and shifts in clade dominance. By comparison, the end-Cretaceous mass extinction was less severe but eliminated several major clades while some rare surviving clades diversified in the Paleogene. This disconnect may be better understood by incorporating the phylogenetic relatedness of taxa into studies of mass extinctions, as the factors driving extinction and recovery are thought to be phylogenetically conserved and should therefore promote both origination and extinction of closely related taxa. Here, we test whether there was phylogenetic selectivity in extinction and origination using brachiopod genera from the Middle Ordovician through the Devonian. Using an index of taxonomic clustering (R_CL) as a proxy for phylogenetic clustering, we find that A) both extinctions and originations shift from taxonomically random or weakly clustered within families in the Ordovician to strongly clustered in the Silurian and Devonian, beginning with the recovery following the Late Ordovician mass extinction, and B) the Late Ordovician mass extinction was itself only weakly clustered. Both results stand in stark contrast to Cretaceous-Cenozoic bivalves, which showed significant levels of taxonomic clustering of extinctions in the Cretaceous, including strong clustering in the mass extinction, but taxonomically random extinctions in the Cenozoic. The contrasting patterns between the Late Ordovician and end-Cretaceous events suggest a complex relationship between the phylogenetic selectivity of mass extinctions and the long-term phylogenetic signal in origination and extinction patterns.     

Inferring the accumulation of morphological disparity in epiphyllous liverworts

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

Bivalves and evolutionary resilience: old skills and new strategies to recover from the P/T and T/J extinction events

Diversity dynamics among bivalves during the Triassic and Early Jurassic provides the opportunity to analyse the recovery patterns after two mass extinctions: Permian/Triassic and Triassic/Jurassic (T/J). The results presented here are based on a newly compiled worldwide genus-level database and are contrasted to the main morphological characters of the different taxonomical (orders and their constituent families and genera) and ecological groups. Many of such morphological characters are innovations appearing during the time span considered. Diversity and evolutionary rates were assessed and compared between these groups. During the Early Triassic there was a slow recovery, dominated by epifaunal taxa, the order Pectinida being the most diverse. The major post-Permian radiation took place during the Anisian, with several morphological and ecological innovations appearing and/or diversifying. The Late Triassic was a time of great diversification and ecological specialisation. Although the T/J was a true mass extinction for bivalves, it was not indiscriminate as its impact was stronger on specialised orders and not all ecological categories were equally affected. Recovery during earliest Jurassic was fast, confirming the high-evolutionary resilience of bivalve molluscs, except for groups with thick shells and tropical distribution, probably because of a biocalcification crisis.     

Morphological and developmental macroevolution: a paleontological perspective

Evidence of the morphological evolution of metazoans has been preserved, in varying degrees of completeness, in the fossil record of the last 600 million years. Although extinction has been incessant at lower taxonomic levels, genomic comparisons among surviving members of higher taxa suggest that much of the developmental systems that pattern their bodyplans has been conserved from early in their history. Comparisons between the origin of morphological disparity in the record and patterns of genomic disparity among living taxa promise to be interesting. For example, Hox cluster composition varies among major taxa, and the fossil record suggests that many of the changes in Hox clusters may have been associated with late Neoproterozoic evolution among minute benthic vermiform clades, from which crown bilaterian phyla arose just before or during the Cambrian explosion. Study of genomic differences among crown classes and orders whosetiming and mode of origin can be inferred from morphological data inthefossil record should throw further light on the timing and mode of origin of genomic disparities.     

Phanerozoic survivors: Actinopterygian evolution through the Permo‐Triassic and Triassic‐Jurassic mass extinction events

Actinopterygians (ray‐finned fishes) successfully passed through four of the big five mass extinction events of the Phanerozoic, but the effects of these crises on the group are poorly understood. Many researchers have assumed that the Permo‐Triassic mass extinction (PTME) and end‐Triassic extinction (ETE) had little impact on actinopterygians, despite devastating many other groups. Here, two morphometric techniques, geometric (body shape) and functional (jaw morphology), are used to assess the effects of these two extinction events on the group. The PTME elicits no significant shifts in functional disparity while body shape disparity increases. An expansion of body shape and functional disparity coincides with the neopterygian radiation and evolution of novel feeding adaptations in the Middle‐Late Triassic. Through the ETE, small decreases are seen in shape and functional disparity, but are unlikely to represent major changes brought about by the extinction event. In the Early Jurassic, further expansions into novel areas of ecospace indicative of durophagy occur, potentially linked to losses in the ETE. As no evidence is found for major perturbations in actinopterygian evolution through either extinction event, the group appears to have been immune to two major environmental crises that were disastrous to most other organisms.