Positive correlation between diversification rates and phenotypic evolvability can mimic punctuated equilibrium on molecular phylogenies

The hypothesis of punctuated equilibrium proposes that most phenotypic evolution occurs in rapid bursts associated with speciation events. Several methods have been developed that can infer punctuated equilibrium from molecular phylogenies in the absence of paleontological data. These methods essentially test whether the variance in phenotypes among extant species is better explained by evolutionary time since common ancestry or by the number of estimated speciation events separating taxa. However, apparent "punctuational" trait change can be recovered on molecular phylogenies if the rate of phenotypic evolution is correlated with the rate of speciation. Strong support for punctuational models can arise even if the underlying mode of trait evolution is strictly gradual, so long as rates of speciation and trait evolution covary across the branches of phylogenetic trees, and provided that lineages vary in their rate of speciation. Species selection for accelerated rates of ecological or phenotypic divergence can potentially lead to the perception that most trait divergence occurs in association with speciation events.     

Detection of punctuated equilibrium from molecular phylogenies

Abstract The theory of ‘punctuated equilibrium’ hypothesises that most morphological change in species takes place in rapid bursts triggered by speciation. Eldregde and Gould postulated the theory in 1972, as an alternative to the idea that morphological change slowly accumulates in the course of time, a then common belief they dubbed ‘phyletic gradualism’. Ever since its introduction the theory of punctuated equilibrium has been the subject of speculation rather than empirical validation. Here I present a method to detect punctuated evolution without reference to fossil data, based on the phenotypes of extant species and on their relatedness as revealed by molecular phylogeny. The method involves a general mathematical model describing morphological differentiation of two species over time. The two parameters in the model, the rates of punctual (cladogenetic) and gradual (anagenetic) change, are estimated from plots of morphological diversification against time since divergence of extant species.     

Rates of morphological evolution are correlated with species richness in salamanders

The tempo and mode of species diversification and phenotypic evolution vary widely across the tree of life, yet the relationship between these processes is poorly known. Previous tests of the relationship between rates of phenotypic evolution and rates of species diversification have assumed that species richness increases continuously through time. If this assumption is violated, simple phylogenetic estimates of net diversification rate may bear no relationship to processes that influence the distribution of species richness among clades. Here, we demonstrate that the variation in species richness among plethodontid salamander clades is unlikely to have resulted from simple time-dependent processes, leading to fundamentally different conclusions about the relationship between rates of phenotypic evolution and species diversification. Morphological evolutionary rates of both size and shape evolution are correlated with clade species richness, but are uncorrelated with simple estimators of net diversification that assume constancy of rates through time. This coupling between species diversification and phenotypic evolution is consistent with the hypothesis that clades with high rates of morphological trait evolution may diversify more than clades with low rates. Our results indicate that assumptions about underlying processes of diversity regulation have important consequences for interpreting macroevolutionary patterns.     

Detection of "punctuated equilibrium" by bayesian estimation of speciation and extinction rates, ancestral character states, and rates of anagenetic and cladogenetic evolution on a molecular phylogeny

Algorithms are presented to simultaneously estimate probabilities of speciation and extinction, rates of anagenetic and cladogenetic phenotypic evolution, as well as ancestral character states, from a complete ultrametric species-level phylogeny with dates assigned to all bifurcations and one or more phenotypes in three or more extant species, using Metropolis-Hastings Markov Chain Monte Carlo sampling. The algorithms also estimate missing phenotypes of extant species and numbers of speciation events that occurred on all branches of the phylogeny. The algorithms are discussed and their performance is evaluated using simulated data. That evaluation shows that precise estimation of rates of evolution of one or a few phenotypes requires large phylogenies. Estimation accuracy improves with the number of species on the phylogeny.     

Ancient and contingent body shape diversification in a hyperdiverse continental fish radiation

The characiform fishes of the Neotropics and Africa radiated remarkably in ecomorphology, but the macroevolutionary processes responsible for their biodiversity remain unexplored, and the degree to which their continental diversification parallels classic adaptive radiations remains untested. We reconstruct their diversification using a new fossil‐calibrated molecular phylogeny, dietary information, and geometric morphometrics. Though body shape diversified early in a manner consistent with an ancient continental adaptive radiation, trophic shifts did not always coincide with shape changes. With the notable exception of piscivores, lineages that converged in diet did not converge closely in body shape. Shifts in habitat or other variables likely influenced body shape evolution in addition to changes in diet, and the clade's history departs from many classic adaptive radiations in lakes or on islands, in which trophic convergence drives morphological convergence. The contrast between the Neotropical radiation's exhaustive exploration of morphospace and the more restrained diversification in Africa suggests a major role for contingency in characiform evolution, with the presence of cypriniform competitors in the Old World, but not the New, providing one possible explanation. Our results depict the clearest ecomorphological reconstruction to date for Characiformes and set the stage for studies further elucidating the processes underlying its diversification.     

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.     

Evidence of constrained phenotypic evolution in a cryptic species complex of agamid lizards

Lineages that exhibit little morphological change over time provide a unique opportunity to explore whether nonadaptive or adaptive processes explain the conservation of morphology over evolutionary time scales. We provide the most comprehensive evaluation to date of the evolutionary processes leading to morphological similarity among species in a cryptic species complex, incorporating two agamid lizard species (Diporiphora magna and D. bilineata). Phylogenetic analysis of mitochondrial (ND2) and nuclear (RAG-1) gene regions revealed the existence of eight deeply divergent clades. Analysis of morphological data confirmed the presence of cryptic species among these clades. Alternative evolutionary hypotheses for the morphological similarity of species were tested using a combination of phylogenetic, morphological, and ecological data. Likelihood model testing of morphological data suggested a history of constrained phenotypic evolution where lineages have a tendency to return to their medial state, whereas ecological data showed support for both Brownian motion and constrained evolution. Thus, there was an overriding signature of constrained evolution influencing morphological divergence between clades. Our study illustrates the utility of using a combination of phylogenetic, morphological, and ecological data to investigate evolutionary mechanisms maintaining cryptic species.     

Energetic benefits and adaptations in mammalian limbs: Scale effects and selective pressures

Differences in limb size and shape are fundamental to mammalian morphological diversity; however, their relevance to locomotor costs has long been subject to debate. In particular, it remains unknown if scale effects in whole limb morphology could partially underlie decreasing mass‐specific locomotor costs with increasing limb length. Whole fore‐ and hindlimb inertial properties reflecting limb size and shape—moment of inertia (MOI), mass, mass distribution, and natural frequency—were regressed against limb length for 44 species of quadrupedal mammals. Limb mass, MOI, and center of mass position are negatively allometric, having a strong potential for lowering mass‐specific locomotor costs in large terrestrial mammals. Negative allometry of limb MOI results in a 40% reduction in MOI relative to isometry's prediction for our largest sampled taxa. However, fitting regression residuals to adaptive diversification models reveals that codiversification of limb mass, limb length, and body mass likely results from selection for differing locomotor modes of running, climbing, digging, and swimming. The observed allometric scaling does not result from selection for energetically beneficial whole limb morphology with increasing size. Instead, our data suggest that it is a consequence of differing morphological adaptations and body size distributions among quadrupedal mammals, highlighting the role of differing limb functions in mammalian evolution.     

Recovering speciation and extinction dynamics based on phylogenies

Phylogenetic trees of only extant species contain information about the underlying speciation and extinction pattern. In this review, I provide an overview over the different methodologies that recover the speciation and extinction dynamics from phylogenetic trees. Broadly, the methods can be divided into two classes: (i) methods using the phylogenetic tree shapes (i.e. trees without branch length information) allowing us to test for speciation rate variation and (ii) methods using the phylogenetic trees with branch length information allowing us to quantify speciation and extinction rates. I end the article with an overview on limitations, open questions and challenges of the reviewed methodology.     

The distribution of mammal body masses

How the diversity of organisms relates to their body sizes has long been a question of interest to biologists, an interest that has grown as data have become available from an increasing number of taxa at ever larger spatial scales. Here, we examine the form of this relationship for a large proportion of the global placental mammal fauna. In common with other large-scale assemblages, the frequency distribution of mammal body masses is strongly right-skewed, even after logarithmic transformation. The modal body mass is slightly lower than predicted by a recent energetic fitness model, but the exact modal value depends on the taxonomic inclusivity of the analyses. Moreover, threatened species are larger bodied than expected by chance, suggesting that extinct species may also have been so. Therefore, the loss of large-bodied species from the global mammalian fauna could potentially have lowered the mode of the distribution. However, this loss must be balanced against evidence that most mammal species for which body mass data were not available for our analyses are small-bodied, which may in turn raise the apparent mode of the distribution. Clearly, tests of explanations for patterns in body size frequency distributions will be complicated by the fact that present-day distributions may be significantly biased by species that are missing from them.     

Deceleration of morphological evolution in a cryptic species complex and its link to paleontological stasis

Morphological stasis or the absence of morphological change is a well-known phenomenon in the paleontological record, yet it is poorly integrated with neontological evidence. Recent evidence suggests that cryptic species complexes may remain morphologically identical due to morphological stasis. Here, we describe a case of long-term stasis in the Stygocapitella cryptic species complex (Parergodrilidae, Orbiniida, Annelida). Using phylogenetic methods and morphological data, we find that rates of morphological evolution in Stygocapitella are significantly slower than in closely related taxa (Nerillidae, Orbiniidae). Assessment of quantitative and qualitative morphology revealed the presence of four morphotypes with only subtle differences, whereas molecular data supports 10 reproductively isolated clades. Notably, estimates for the time of Stygocapitella species divergence range from ∼275 million years to ∼18 million years, including one case of two morphologically similar species that have diverged about 140 million years ago. These findings provide evidence for morphological deceleration and long-term morphological stasis in Stygocapitella, and that speciation is not necessarily accompanied by morphological changes. The deceleration of morphological divergence in Stygocapitella can be potentially linked to niche conservatism and tracking, coupled with the fluctuating dynamics of the interstitial environment, or genetic constraints due to progenetic evolution. Finally, we conclude that failing to integrate speciation without morphological evolution in paleontology may bias estimates of rates of speciation and morphological evolution.     

Exceptional avian herbivores: multiple transitions toward herbivory in the bird order Anseriformes and its correlation with body mass

Herbivory is rare among birds and is usually thought to have evolved predominately among large, flightless birds due to energetic constraints or an association with increased body mass. Nearly all members of the bird order Anseriformes, which includes ducks, geese, and swans, are flighted and many are predominately herbivorous. However, it is unknown whether herbivory represents a derived state for the order and how many times a predominately herbivorous diet may have evolved. Compiling data from over 200 published diet studies to create a continuous character for herbivory, models of trait evolution support at least five independent transitions toward a predominately herbivorous diet in Anseriformes. Although a nonphylogenetic correlation test recovers a significant positive correlation between herbivory and body mass, this correlation is not significant when accounting for phylogeny. These results indicate a lack of support for the hypothesis that a larger body mass confers an advantage in the digestion of low‐quality diets but does not exclude the possibility that shifts to a more abundant food source have driven shifts toward herbivory in other bird lineages. The exceptional number of transitions toward a more herbivorous diet in Anseriformes and lack of correlation with body mass prompts a reinterpretation of the relatively infrequent origination of herbivory among flighted birds.     

ORIGIN AND DIVERSIFICATION OF THE CALIFORNIA FLORA: RE‐EXAMINING CLASSIC HYPOTHESES WITH MOLECULAR PHYLOGENIES

The California Floristic Province exhibits one of the richest floras on the planet, with more than 5500 native plant species, approximately 40% of which are endemic. Despite its impressive diversity and the attention it has garnered from ecologists and evolutionary biologists, historical causes of species richness and endemism in California remain poorly understood. Using a phylogenetic analysis of 16 angiosperm clades, each containing California natives in addition to species found only outside California, we show that CA's current biodiversity primarily results from low extinction rates, as opposed to elevated speciation or immigration rates. Speciation rates in California were lowest among Arcto‐Tertiary lineages (i.e., those colonizing California from the north, during the Tertiary), but extinction rates were universally low across California native plants of all historical, geographic origins. In contrast to long‐accepted ideas, we find that California diversification rates were generally unaffected by the onset of the Mediterranean climate. However, the Mediterranean climate coincided with immigration of many desert species, validating one previous hypothesis regarding origins of CA's plant diversity. This study implicates topographic complexity and climatic buffering as key, long‐standing features of CA's landscape favoring plant species persistence and diversification, and highlights California as an important refuge under changing climates.     

A statistical test of unbiased evolution of body size in birds

Abstract.— Of the approximately 9500 bird species, the vast majority is small-bodied. That is a general feature of evolutionary lineages, also observed for instance in mammals and plants. The avian interspecific body size distribution is right-skewed even on a logarithmic scale. That has previously been interpreted as evidence that body size evolution has been biased. However, a procedure to test for unbiased evolution from the shape of body size distributions was lacking. In the present paper unbiased body size evolution is defined precisely, and a statistical test is developed based on Monte Carlo simulation of unbiased evolution. Application of the test to birds suggests that it is highly unlikely that avian body size evolution has been unbiased as defined. Several possible explanations for this result are discussed. A plausible explanation is that the general model of unbiased evolution assumes that population size and generation time do not affect the evolutionary variability of body size; that is, that micro- and macroevolution are decoupled, which theory suggests is not likely to be the case.     

Predicting speciation probability from replicated population histories

In this issue of Molecular Ecology, Yamasaki et al. (2020) use genetic data from extensive sampling of Rhinogobius goby fish across the Ryukyu Archipelago in Japan to demonstrate the parallel speciation of a freshwater form from an ancestral amphidromous form. They then show that ecosystem size strongly predicts the probability of speciation between the two forms across islands. In doing so, this study connects population‐level processes (microevolution) to broad‐scale biodiversity patterns (macroevolution), an important but understudied link in evolutionary biology. Moving forward, we can build on this research to (a) more directly determine how geographic, ecological and historical factors influence the different stages of the speciation process, and (b) understand whether mechanisms inferred from insular radiations extend to those on continents, where both demographic histories and environmental regimes are likely more complex.     

Phylogenetic signal in the evolution of body colour and spicule skeleton in calcareous sponges

Some of the morphological characters used in Porifera taxonomy have often been shown to be inconsistent. In the present study, we tested the phylogenetic coherence of currently used taxonomic characters of the calcarean genus Clathrina. For this, 20 species of Clathrina and three other calcinean genera (Ascandra, Guancha, and Leucetta) were sequenced for the ITS and D2 region of the 28S ribosomal DNA. Maximum‐likelihood and maximum‐parsimony algorithms were used to reconstruct phylogenetic trees. Deep divergences were observed in our tree and Clathrina was shown to be paraphyletic. The major split in our topology showed a clear‐cut distinction between sponges with and without tetractine spicules. Moreover, a group of yellow‐coloured Clathrina was clearly separated from the remaining white‐coloured species. Our results show that the presence of diactines, water‐collecting tubes, the degree of cormus anastomosis, and actine shapes do not correlate with the major clades of the calcinean phylogeny. On the other hand, the presence of tripods, the absence of tetractines, and the presence of spines in the apical actine of tetractines seem to be good synapomorphies for clades in our tree. Our results demonstrate that skeleton characters can be reliably used in higher level taxonomy in Clathrinida. © 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163 , 1026–1034.     

Phylogenetic structure of mammal assemblages at large geographical scales: linking phylogenetic community ecology with macroecology

Phylogenetic community ecology seeks to explain the processes involved in the formation of species assemblages by analysing their phylogenetic structure, and to date has focused primarily on local-scale communities. Macroecology, on the other hand, is concerned with the structure of assemblages at large geographical scales, but has remained largely non-phylogenetic. Analysing the phylogenetic structure of large-scale assemblages provides a link between these two research programmes. In this paper, I ask whether we should expect large-scale assemblages to show significant phylogenetic structure, by outlining some of the ecological and macroevolutionary processes that may play a role in assemblage formation. As a case study, I then explore the phylogenetic structure of carnivore assemblages within the terrestrial ecoregions of Africa. Many assemblages at these scales are indeed phylogenetically non-random (either clustered or overdispersed). One interpretation of the observed patterns of phylogenetic structure is that many clades underwent rapid biome-filling radiations, followed by diversification slowdown and competitive sorting as niche space became saturated.     

Why do species exist? Insights from sexuals and asexuals

Why does life diversify into the more or less discrete entities we recognise as species? Two main explanations have been proposed: i) species are a consequence of adaptation to different ecological niches, ii) species are a consequence of sexual reproduction and reproductive isolation. Phylogenetic studies of case-study groups can provide insights into the relative importance of divergent selection and isolation for speciation, but it can be difficult to infer causes of speciation unambiguously. The example of North American tiger beetles from the genus Cicindela is discussed. An alternative approach is to compare diversification between related sexual and asexual taxa to infer the relative importance of the two explanations. We outline expected patterns of diversification in sexual and asexual lineages under different scenarios using coalescent theory. Whether sexuals or asexuals diversify to a greater extent depends on the balance among various stages of diversification, particularly on the effects of sexual reproduction on rates of adaptive evolution. Rotifers offer a unique system to test these ideas, allowing comparison of patterns of genetic and functional morphological diversification in sexual (bdelloid) and asexual (monogonont) clades.     

MORPHOLOGICAL RATES OF ANGIOSPERM SEED SIZE EVOLUTION

The evolution of seed size among angiosperms reflects their ecological diversification in a complex fitness landscape of life‐history strategies. The lineages that have evolved seeds beyond the upper and lower boundaries that defined nonflowering seed plants since the Paleozoic are more dispersed across the angiosperm phylogeny than would be expected under a neutral model of phenotypic evolution. Morphological rates of seed size evolution estimated for 40 clades based on 17,375 species ranged from 0.001 (Garryales) to 0.207 (Malvales). Comparative phylogenetic analysis indicated that morphological rates are not associated with the clade's seed size but are negatively correlated with the clade's position in the overall distribution of angiosperm seed sizes; clades with seed sizes closer to the angiosperm mean had significantly higher morphological rates than clades with extremely small or extremely large seeds. Likewise, per‐clade taxonomic diversification rates are not associated with the seed size of the clade but with where the clade falls within the angiosperm seed size distribution. These results suggest that evolutionary rates (morphological and taxonomic) are elevated in densely occupied regions of the seed morphospace relative to lineages whose ecophenotypic innovations have moved them toward the edges.