Macroevolutionary thermodynamics: Temperature and the tempo of evolution in the tropics

An influential hypothesis proposes that the tempo of evolution is faster in the tropics. Emerging evidence, including a study in this issue of PLOS Biology, challenges this view, raising new questions about the causes of Earth’s iconic latitudinal diversity gradient (LDG).

Biologists have long puzzled over the spectacular diversity of animals and plants from Earth’s tropical regions. It is true that some tropical environments are not especially rich in species, and some groups of organisms show contrarian patterns with diversity peaks that occur far outside of the warm, humid tropics. Nonetheless, the big picture is clear: A vastly disproportionate fraction of Earth’s terrestrial biodiversity is concentrated in tropical rainforests, and warm water reef environments similarly account for a large fraction of marine diversity. The extremes of tropical diversity transcend the ability of most humans to process it: Some Amazonian rainforests, for example, contain more species of trees in just a few hectares than are found in the entirety of Europe or North America [1]. In general, the most diverse tropical rainforests support order-of-magnitude increases in species richness relative to otherwise comparable temperate zone communities across a wide range of organisms. Despite decades of study, however, the causes of this latitudinal diversity gradient (LDG) remain elusive.One of the most prominent hypotheses for the LDG is, loosely speaking, the idea that biological processes speed up in the tropics, potentially due to the kinetic effects of temperature on the rates of organismal processes. It seems obvious that the pulse of life should be faster under a torrid tropical sun, and—to naturalists who’ve spent time in lowland rainforests in particular—such a view accords well with perceptions of the humid tropics as a raging, steamy mess of species interactions that collectively generate the tangled web that is tropical diversity. It is generally accepted that temperature can affect metabolic rate and many other biological processes, including those involving ecological interactions between species (e.g., competition, predation, and herbivory). The specific mechanisms connecting thermal energy to biodiversity remain unclear. For example, they might involve the influence of temperature on rates of molecular evolution, which might then influence rates of speciation [2]. Or, species in warmer environments might live closer to their optimal body temperatures, thus enabling them to allocate more resources to performance-associated functions and leading to a systematic upgrading in the intensity of antagonistic or coevolutionary interactions between species [3]. Regardless of the specific mechanism, the general idea is captured by Brown [4], who notes that “‘Diversity begets diversity’ in the tropics, because ‘the Red Queen runs faster when she is hot.’”Writing in PLOS Biology, Drury and colleagues [5] demonstrate that a central prediction of these “faster tropics” hypotheses fails to hold up. They predicted that, if certain types of ecological interactions between species are stronger in the tropics, then we should see a signal of those interactions in long-term patterns of trait evolution. In particular, the increased pressure to respond to species interactions in the tropics should result in faster overall rates of morphological evolution for tropical species. To test this hypothesis, the authors studied the rate of morphological evolution in birds, analyzing a large dataset on bill shape and body proportions from other recent studies [6] with a battery of sophisticated statistical models. These models allowed the rate of morphological change to differ systematically with latitude. Intriguingly, the models that best fit the data in some cases were those that allowed for strong interactions between species in driving patterns of divergence among closely related species that occupied that same biogeographic region (e.g., the neotropics). Thus, there is a partial signal of species interactions on the morphologies of species we see living together today, including those from both tropical and temperate regions. As suggested by the authors, these patterns might reflect a form of ecological character displacement, whereby morphologically similar species evolve differences that minimize their ecological overlap. But, surprisingly, the intensity of these effects shows no consistent relationship with latitude. The take-home message is that—at least for birds and the traits considered—species are not evolving more rapidly in the tropics.Drury and colleagues note that their results contradict recent articles that have documented differences in phenotypic evolutionary rates across latitude, although the studies referenced generally looked at different types of traits (e.g., birdsong). They suggest several potential reasons for the discrepancies between their results and those prior studies. But, critically, these earlier studies generally did not report faster evolution in the tropics, but faster evolution in the temperate zone. Hence, the results of Drury and colleagues and the earlier studies all converge to a similar and more general finding, which is that the warm tropics really aren’t so hot for macroevolution, at least as far as phenotypic evolutionary rates are concerned. By rejecting the simple explanations (faster evolution), new questions emerge about how and why tropical bird communities show such dramatic phenotypic and ecological diversity.Morphological evolution is not the only process that fails to show the expected pattern of “heating up” in the tropics. A number of recent studies have found that rates of species formation are either unrelated to latitude or slower in the tropics [7–9]. These results argue strongly against temperature kinetic models of biodiversity, whereby faster speciation emerges from the effects of warmer temperatures in the tropics on mutation and metabolic rates [10]. Many of the same causal pathways that predict increased rates of speciation as a function of temperature would also apply to rates of morphological evolution: Increased mutation rates in the tropics, for example, should accelerate the tempo of phenotypic evolution due to increased mutational variance in traits. But, regardless of whether we consider phenotypic evolution (as in Drury and colleagues) or lineage diversification, there is simply no evidence for faster evolutionary rates in the tropics.The results from Drury and colleagues [5] and other studies do not reject all possible causal pathways by which temperature or species interactions might facilitate high tropical diversity. Many phylogeny-based studies of species diversification and phenotypic evolution frame their interpretations through the lens of interspecific competition, ecological opportunity, and character displacement. Yet, numerous other types of interactions are relevant to global biodiversity patterns, and some of these interactions have scarcely been explored from a macroevolutionary perspective. Many such interactions have the potential to influence species richness and ecological diversity, perhaps through mechanisms that involve an indirect effect of temperature on equilibrium diversity levels. With more data on how host–pathogen, predator–prey, and other biotic interactions vary latitudinally, perhaps we will emerge with a greater understanding of the diverse mechanisms that contribute to the spectacular enrichment of tropical diversity.     

The signature of competition in ecomorphological traits across the avian radiation

Competition for shared resources represents a fundamental driver of biological diversity. However, the tempo and mode of phenotypic evolution in deep-time has been predominantly investigated using trait evolutionary models which assume that lineages evolve independently from each other. Consequently, the role of species interactions in driving macroevolutionary dynamics remains poorly understood. Here, we quantify the prevalence for signatures of competition between related species in the evolution of ecomorphological traits across the bird radiation. We find that mechanistic trait models accounting for the effect of species interactions on phenotypic divergence provide the best fit for the data on at least one trait axis in 27 out of 59 clades ranging between 21 and 195 species. Where it occurs, the signature of competition generally coincides with positive species diversity-dependence, driven by the accumulation of lineages with similar ecologies, and we find scarce evidence for trait-dependent or negative diversity-dependent phenotypic evolution. Overall, our results suggest that the footprint of interspecific competition is often eroded in long-term patterns of phenotypic diversification, and that other selection pressures may predominantly shape ecomorphological diversity among extant species at macroevolutionary scales.     

Delimiting Species without Nuclear Monophyly in Madagascar's Mouse Lemurs

Background

Speciation begins when populations become genetically separated through a substantial reduction in gene flow, and it is at this point that a genetically cohesive set of populations attain the sole property of species: the independent evolution of a population-level lineage. The comprehensive delimitation of species within biodiversity hotspots, regardless of their level of divergence, is important for understanding the factors that drive the diversification of biota and for identifying them as targets for conservation. However, delimiting recently diverged species is challenging due to insufficient time for the differential evolution of characters—including morphological differences, reproductive isolation, and gene tree monophyly—that are typically used as evidence for separately evolving lineages.

Methodology

In this study, we assembled multiple lines of evidence from the analysis of mtDNA and nDNA sequence data for the delimitation of a high diversity of cryptically diverged population-level mouse lemur lineages across the island of Madagascar. Our study uses a multi-faceted approach that applies phylogenetic, population genetic, and genealogical analysis for recognizing lineage diversity and presents the most thoroughly sampled species delimitation of mouse lemur ever performed.

Conclusions

The resolution of a large number of geographically defined clades in the mtDNA gene tree provides strong initial evidence for recognizing a high diversity of population-level lineages in mouse lemurs. We find additional support for lineage recognition in the striking concordance between mtDNA clades and patterns of nuclear population structure. Lineages identified using these two sources of evidence also exhibit patterns of population divergence according to genealogical exclusivity estimates. Mouse lemur lineage diversity is reflected in both a geographically fine-scaled pattern of population divergence within established and geographically widespread taxa, as well as newly resolved patterns of micro-endemism revealed through expanded field sampling into previously poorly and well-sampled regions.     

Diversity and host assemblage of avian haemosporidians in different terrestrial ecoregions of Peru

Characterizing the diversity and structure of host–parasite communities is crucial to understanding their eco-evolutionary dynamics. Malaria and related haemosporidian parasites are responsible for fitness loss and mortality in bird species worldwide. However, despite exhibiting the greatest ornithological biodiversity, avian haemosporidians from Neotropical regions are quite unexplored. Here, we analyze the genetic diversity of bird haemosporidian parasites (Plasmodium and Haemoproteus) in 1,336 individuals belonging to 206 bird species to explore for differences in diversity of parasite lineages and bird species across 5 well-differentiated Peruvian ecoregions. We detected 70 different haemosporidian lineages infecting 74 bird species. We showed that 25 out of the 70 haplotypes had not been previously recorded. Moreover, we also identified 81 new host–parasite interactions representing new host records for these haemosporidian parasites. Our outcomes revealed that the effective diversity (as well as the richness, abundance, and Shannon–Weaver index) for both birds and parasite lineages was higher in Amazon basin ecoregions. Furthermore, we also showed that ecoregions with greater diversity of bird species also had high parasite richness, hence suggesting that host community is crucial in explaining parasite richness. Generalist parasites were found in ecoregions with lower bird diversity, implying that the abundance and richness of hosts may shape the exploitation strategy followed by haemosporidian parasites. These outcomes reveal that Neotropical region is a major reservoir of unidentified haemosporidian lineages. Further studies analyzing host distribution and specificity of these parasites in the tropics will provide important knowledge about phylogenetic relationships, phylogeography, and patterns of evolution and distribution of haemosporidian parasites.     

Pleiotropic constraints promote the evolution of cooperation in cellular groups

The evolution of cooperation in cellular groups is threatened by lineages of cheaters that proliferate at the expense of the group. These cell lineages occur within microbial communities, and multicellular organisms in the form of tumours and cancer. In contrast to an earlier study, here we show how the evolution of pleiotropic genetic architectures—which link the expression of cooperative and private traits—can protect against cheater lineages and allow cooperation to evolve. We develop an age-structured model of cellular groups and show that cooperation breaks down more slowly within groups that tie expression to a private trait than in groups that do not. We then show that this results in group selection for pleiotropy, which strongly promotes cooperation by limiting the emergence of cheater lineages. These results predict that pleiotropy will rapidly evolve, so long as groups persist long enough for cheater lineages to threaten cooperation. Our results hold when pleiotropic links can be undermined by mutations, when pleiotropy is itself costly, and in mixed-genotype groups such as those that occur in microbes. Finally, we consider features of multicellular organisms—a germ line and delayed reproductive maturity—and show that pleiotropy is again predicted to be important for maintaining cooperation. The study of cancer in multicellular organisms provides the best evidence for pleiotropic constraints, where abberant cell proliferation is linked to apoptosis, senescence, and terminal differentiation. Alongside development from a single cell, we propose that the evolution of pleiotropic constraints has been critical for cooperation in many cellular groups.

The evolution of cooperation in cellular groups is threatened by lineages of cheaters that proliferate at the expense of the group. In this study, an age-structured model of cellular groups shows that pleiotropy promotes the evolution of cooperation and may have been important for the origins of multicellularity.     

Trophic convergence drives morphological convergence in marine tetrapods

Marine tetrapod clades (e.g. seals, whales) independently adapted to marine life through the Mesozoic and Caenozoic, and provide iconic examples of convergent evolution. Apparent morphological convergence is often explained as the result of adaptation to similar ecological niches. However, quantitative tests of this hypothesis are uncommon. We use dietary data to classify the feeding ecology of extant marine tetrapods and identify patterns in skull and tooth morphology that discriminate trophic groups across clades. Mapping these patterns onto phylogeny reveals coordinated evolutionary shifts in diet and morphology in different marine tetrapod lineages. Similarities in morphology between species with similar diets—even across large phylogenetic distances—are consistent with previous hypotheses that shared functional constraints drive convergent evolution in marine tetrapods.     

Phylogenomic assessment of the role of hybridization and introgression in trait evolution

Trait evolution among a set of species—a central theme in evolutionary biology—has long been understood and analyzed with respect to a species tree. However, the field of phylogenomics, which has been propelled by advances in sequencing technologies, has ushered in the era of species/gene tree incongruence and, consequently, a more nuanced understanding of trait evolution. For a trait whose states are incongruent with the branching patterns in the species tree, the same state could have arisen independently in different species (homoplasy) or followed the branching patterns of gene trees, incongruent with the species tree (hemiplasy). Another evolutionary process whose extent and significance are better revealed by phylogenomic studies is gene flow between different species. In this work, we present a phylogenomic method for assessing the role of hybridization and introgression in the evolution of polymorphic or monomorphic binary traits. We apply the method to simulated evolutionary scenarios to demonstrate the interplay between the parameters of the evolutionary history and the role of introgression in a binary trait’s evolution (which we call xenoplasy). Very importantly, we demonstrate, including on a biological data set, that inferring a species tree and using it for trait evolution analysis in the presence of gene flow could lead to misleading hypotheses about trait evolution.     

Environmental variation is a major predictor of global trait turnover in mammals

Aim

To evaluate how environment and evolutionary history interact to influence global patterns of mammal trait diversity (a combination of 14 morphological and life‐history traits).

Location

The global terrestrial environment.

Taxon

Terrestrial mammals.

Methods

We calculated patterns of spatial turnover for mammalian traits and phylogenetic lineages using the mean nearest taxon distance. We then used a variance partitioning approach to establish the relative contribution of trait conservatism, ecological adaptation and clade specific ecological preferences on global trait turnover.

Results

We provide a global scale analysis of trait turnover across mammalian terrestrial assemblages, which demonstrates that phylogenetic turnover by itself does not predict trait turnover better than random expectations. Conversely, trait turnover is consistently more strongly associated with environmental variation than predicted by our null models. The influence of clade‐specific ecological preferences, reflected by the shared component of phylogenetic turnover and environmental variation, was considerably higher than expectations. Although global patterns of trait turnover are dependent on the trait under consideration, there is a consistent association between trait turnover and environmental predictive variables, regardless of the trait considered.

Main conclusions

Our results suggest that changes in phylogenetic composition are not always coupled with changes in trait composition on a global scale and that environmental conditions are strongly associated with patterns of trait composition across species assemblages, both within and across phylogenetic clades.     

Eusociality Shapes Convergent Patterns of Molecular Evolution across Mitochondrial Genomes of Snapping Shrimps

Eusociality is a highly conspicuous and ecologically impactful behavioral syndrome that has evolved independently across multiple animal lineages. So far, comparative genomic analyses of advanced sociality have been mostly limited to insects. Here, we study the only clade of animals known to exhibit eusociality in the marine realm—lineages of socially diverse snapping shrimps in the genus Synalpheus. To investigate the molecular impact of sociality, we assembled the mitochondrial genomes of eight Synalpheus species that represent three independent origins of eusociality and analyzed patterns of molecular evolution in protein-coding genes. Synonymous substitution rates are lower and potential signals of relaxed purifying selection are higher in eusocial relative to noneusocial taxa. Our results suggest that mitochondrial genome evolution was shaped by eusociality-linked traits—extended generation times and reduced effective population sizes that are hallmarks of advanced animal societies. This is the first direct evidence of eusociality impacting genome evolution in marine taxa. Our results also strongly support the idea that eusociality can shape genome evolution through profound changes in life history and demography.     

Deep and wide valleys drive nested phylogeographic patterns across a montane bird community

Montane species distributions interrupted by valleys can lead to range fragmentation, differentiation and ultimately speciation. Paleoclimatic fluctuations may accentuate or reduce such diversification by temporally altering the extent of montane habitat and may affect species differentially. We examined how an entire montane bird community of the Western Ghats—a linear, coastal tropical mountain range—responds to topographic valleys that host different habitats. Using genetic data from 23 species (356 individuals) collected across nine locations, we examined if different species in the community reveal spatial concordance in population differentiation, and whether the timing of these divergences correlate with climatic events. Our results reveal a nested effect of valleys, with several species (10 of 23) demonstrating the oldest divergences associated with the widest and deepest valley in the mountain range, the Palghat Gap. Further, a subset of these 10 species revealed younger divergences across shallower, narrower valleys. We recovered discordant divergence times for all valley-affected montane birds, mostly in the Pleistocene, supporting the Pliestocene-pump hypotheses and highlighting the role of climatic fluctuations during this period in driving species evolution. A majority of species remain unaffected by valleys, perhaps owing to geneflow or extinction–recolonization dynamics. Studying almost the entire community allowed us to uncover a range of species’ responses, including some generalizable and other unpredicted patterns.     

Identification of major quantitative trait loci underlying floral pollination syndrome divergence in Penstemon

Distinct floral pollination syndromes have emerged multiple times during the diversification of flowering plants. For example, in western North America, a hummingbird pollination syndrome has evolved more than 100 times, generally from within insect-pollinated lineages. The hummingbird syndrome is characterized by a suite of floral traits that attracts and facilitates pollen movement by hummingbirds, while at the same time discourages bee visitation. These floral traits generally include large nectar volume, red flower colour, elongated and narrow corolla tubes and reproductive organs that are exerted from the corolla. A handful of studies have examined the genetic architecture of hummingbird pollination syndrome evolution. These studies find that mutations of relatively large effect often explain increased nectar volume and transition to red flower colour. In addition, they suggest that adaptive suites of floral traits may often exhibit a high degree of genetic linkage, which could facilitate their fixation during pollination syndrome evolution. Here, we explore these emerging generalities by investigating the genetic basis of floral pollination syndrome divergence between two related Penstemon species with different pollination syndromes—bee-pollinated P. neomexicanus and closely related hummingbird-pollinated P. barbatus. In an F₂ mapping population derived from a cross between these two species, we characterized the effect size of genetic loci underlying floral trait divergence associated with the transition to bird pollination, as well as correlation structure of floral trait variation. We find the effect sizes of quantitative trait loci for adaptive floral traits are in line with patterns observed in previous studies, and find strong evidence that suites of floral traits are genetically linked. This linkage may be due to genetic proximity or pleiotropic effects of single causative loci. Interestingly, our data suggest that the evolution of floral traits critical for hummingbird pollination was not constrained by negative pleiotropy at loci that show co-localization for multiple traits.     

Weather, not climate, defines distributions of vagile bird species

Background

Accurate predictions of species distributions are essential for climate change impact assessments. However the standard practice of using long-term climate averages to train species distribution models might mute important temporal patterns of species distribution. The benefit of using temporally explicit weather and distribution data has not been assessed. We hypothesized that short-term weather associated with the time a species was recorded should be superior to long-term climate measures for predicting distributions of mobile species.

Methodology

We tested our hypothesis by generating distribution models for 157 bird species found in Australian tropical savannas (ATS) using modelling algorithm Maxent. The variable weather of the ATS supports a bird assemblage with variable movement patterns and a high incidence of nomadism. We developed “weather” models by relating climatic variables (mean temperature, rainfall, rainfall seasonality and temperature seasonality) from the three month, six month and one year period preceding each bird record over a 58 year period (1950–2008). These weather models were compared against models built using long-term (30 year) averages of the same climatic variables.

Conclusions

Weather models consistently achieved higher model scores than climate models, particularly for wide-ranging, nomadic and desert species. Climate models predicted larger range areas for species, whereas weather models quantified fluctuations in habitat suitability across months, seasons and years. Models based on long-term climate averages over-estimate availability of suitable habitat and species'' climatic tolerances, masking species potential vulnerability to climate change. Our results demonstrate that dynamic approaches to distribution modelling, such as incorporating organism-appropriate temporal scales, improves understanding of species distributions.     

Habitat use affects morphological diversification in dragon lizards

Habitat use may lead to variation in diversity among evolutionary lineages because habitats differ in the variety of ways they allow for species to make a living. Here, we show that structural habitats contribute to differential diversification of limb and body form in dragon lizards (Agamidae). Based on phylogenetic analysis and ancestral state reconstructions for 90 species, we find that multiple lineages have independently adopted each of four habitat use types: rock‐dwelling, terrestriality, semi‐arboreality and arboreality. Given these reconstructions, we fit models of evolution to species’ morphological trait values and find that rock‐dwelling and arboreality limit diversification relative to terrestriality and semi‐arboreality. Models preferred by Akaike information criterion infer slower rates of size and shape evolution in lineages inferred to occupy rocks and trees, and model‐averaged rate estimates are slowest for these habitat types. These results suggest that ground‐dwelling facilitates ecomorphological differentiation and that use of trees or rocks impedes diversification.     

Phylogenetic perspectives on reef fish functional traits

Functional traits have been fundamental to the evolution and diversification of entire fish lineages on coral reefs. Yet their relationship with the processes promoting speciation, extinction and the filtering of local species pools remains unclear. We review the current literature exploring the evolution of diet, body size, water column use and geographic range size in reef‐associated fishes. Using published and new data, we mapped functional traits on to published phylogenetic trees to uncover evolutionary patterns that have led to the current functional diversity of fishes on coral reefs. When examining reconstructed patterns for diet and feeding mode, we found examples of independent transitions to planktivory across different reef fish families. Such transitions and associated morphological alterations may represent cases in which ecological opportunity for the exploitation of different resources drives speciation and adaptation. In terms of body size, reconstructions showed that both large and small sizes appear multiple times within clades of mid‐sized fishes and that extreme body sizes have arisen mostly in the last 10 million years (Myr). The reconstruction of range size revealed many cases of disparate range sizes among sister species. Such range size disparity highlights potential vicariant processes through isolation in peripheral locations. When accounting for peripheral speciation processes in sister pairs, we found a significant relationship between labrid range size and lineage age. The diversity and evolution of traits within lineages is influenced by trait–environment interactions as well as by species and trait–trait interactions, where the presence of a given trait may trigger the development of related traits or behaviours. Our effort to assess the evolution of functional diversity across reef fish clades adds to the burgeoning research focusing on the evolutionary and ecological roles of functional traits. We argue that the combination of a phylogenetic and a functional approach will improve the understanding of the mechanisms of species assembly in extraordinarily rich coral reef communities.     

A Second Dimension to the Leaf Economics Spectrum Predicts Edaphic Habitat Association in a Tropical Forest

Background

Strong patterns of habitat association are frequent among tropical forest trees and contribute to the maintenance of biodiversity. The relation of edaphic differentiation to tradeoffs among leaf functional traits is less clear, but may provide insights into mechanisms of habitat partitioning in these species rich assemblages.

Methodology/Principal Findings

We quantify the leaf economics spectrum (LES) for 16 tree species within a Bornean forest characterized by highly pronounced habitat specialization. Our findings suggest that the primary axis of trait variation in light-limited, lowland tropical forests was identical to the LES and corresponds with the shade tolerance continuum. There was no separation with respect to edaphic variation along this primary axis of trait variation. However, a second orthogonal axis determined largely by foliar P concentrations resulted in a near-perfect separation of species occupying distinct soil types within the forest.

Conclusions/Significance

We suggest that this second axis of leaf trait variation represents a “leaf edaphic habitat spectrum” related to foliar P and potentially other nutrients closely linked to geological substrate, and may generally occur in plant communities characterized by strong edaphic resource gradients.     

Three-dimensional geometric morphometric analysis of the skull of Protoceratops andrewsi supports a socio-sexual signalling role for the ceratopsian frill

Socio-sexual selection is predicted to be an important driver of evolution, influencing speciation, extinction and adaptation. The fossil record provides a means of testing these predictions, but detecting its signature from morphological data alone is difficult. There are, nonetheless, some specific patterns of growth and variation which are expected of traits under socio-sexual selection. The distinctive parietal-squamosal frill of ceratopsian dinosaurs has previously been suggested as a socio-sexual display trait, but evidence for this has been limited. Here, we perform a whole-skull shape analysis of an unprecedentedly large sample of specimens of Protoceratops andrewsi using a high-density landmark-based geometric morphometric approach to test four predictions regarding a potential socio-sexual signalling role for the frill. Three predictions—low integration with the rest of the skull, significantly higher rate of change in size and shape during ontogeny, and higher morphological variance than other skull regions—are supported. One prediction, sexual dimorphism in shape, is not supported, suggesting that sexual differences in P. andrewsi are likely to be small. Together, these findings are consistent with mutual mate choice or selection for signalling quality in more general social interactions, and support the hypothesis that the frill functioned as a socio-sexual signal in ceratopsian dinosaurs.     

Morphometric Relationship,Phylogenetic Correlation,and Character Evolution in the Species-Rich Genus Aphis (Hemiptera: Aphididae)

Background

The species-rich genus Aphis consists of more than 500 species, many of them host-specific on a wide range of plants, yet very similar in general appearance due to convergence toward particular morphological types. Most species have been historically clustered into four main phenotypic groups (gossypii, craccivora, fabae, and spiraecola groups). To confirm the morphological hypotheses between these groups and to examine the characteristics that determine them, multivariate morphometric analyses were performed using 28 characters measured/counted from 40 species. To infer whether the morphological relationships are correlated with the genetic relationships, we compared the morphometric dataset with a phylogeny reconstructed from the combined dataset of three mtDNA and one nuclear DNA regions.

Principal Findings

Based on a comparison of morphological and molecular datasets, we confirmed morphological reduction or regression in the gossypii group unlike in related groups. Most morphological characteristics of the gossypii group were less variable than for the other groups. Due to these, the gossypii group could be morphologically well separated from the craccivora, fabae, and spiraecola groups. In addition, the correlation of the rates of evolution between morphological and DNA datasets was highly significant in their diversification.

Conclusions

The morphological separation between the gossypii group and the other species-groups are congruent with their phylogenetic relationships. Analysis of trait evolution revealed that the morphological traits found to be significant based on the morphometric analyses were confidently correlated with the phylogeny. The dominant patterns of trait evolution resulting in increased rates of short branches and temporally later evolution are likely suitable for the modality of Aphis speciation because they have adapted species-specifically, rapidly, and more recently on many different host plants.     

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.     

Opposing community assembly patterns for dominant and nondominant plant species in herbaceous ecosystems globally

Biotic and abiotic factors interact with dominant plants—the locally most frequent or with the largest coverage—and nondominant plants differently, partially because dominant plants modify the environment where nondominant plants grow. For instance, if dominant plants compete strongly, they will deplete most resources, forcing nondominant plants into a narrower niche space. Conversely, if dominant plants are constrained by the environment, they might not exhaust available resources but instead may ameliorate environmental stressors that usually limit nondominants. Hence, the nature of interactions among nondominant species could be modified by dominant species. Furthermore, these differences could translate into a disparity in the phylogenetic relatedness among dominants compared to the relatedness among nondominants. By estimating phylogenetic dispersion in 78 grasslands across five continents, we found that dominant species were clustered (e.g., co‐dominant grasses), suggesting dominant species are likely organized by environmental filtering, and that nondominant species were either randomly assembled or overdispersed. Traits showed similar trends for those sites (<50%) with sufficient trait data. Furthermore, several lineages scattered in the phylogeny had more nondominant species than expected at random, suggesting that traits common in nondominants are phylogenetically conserved and have evolved multiple times. We also explored environmental drivers of the dominant/nondominant disparity. We found different assembly patterns for dominants and nondominants, consistent with asymmetries in assembly mechanisms. Among the different postulated mechanisms, our results suggest two complementary hypotheses seldom explored: (1) Nondominant species include lineages adapted to thrive in the environment generated by dominant species. (2) Even when dominant species reduce resources to nondominant ones, dominant species could have a stronger positive effect on some nondominants by ameliorating environmental stressors affecting them, than by depleting resources and increasing the environmental stress to those nondominants. These results show that the dominant/nondominant asymmetry has ecological and evolutionary consequences fundamental to understand plant communities.     

The selfing syndrome: a model for studying the genetic and evolutionary basis of morphological adaptation in plants

Background

In angiosperm evolution, autogamously selfing lineages have been derived from outbreeding ancestors multiple times, and this transition is regarded as one of the most common evolutionary tendencies in flowering plants. In most cases, it is accompanied by a characteristic set of morphological and functional changes to the flowers, together termed the selfing syndrome. Two major areas that have changed during evolution of the selfing syndrome are sex allocation to male vs. female function and flower morphology, in particular flower (mainly petal) size and the distance between anthers and stigma.

Scope

A rich body of theoretical, taxonomic, ecological and genetic studies have addressed the evolutionary modification of these two trait complexes during or after the transition to selfing. Here, we review our current knowledge about the genetics and evolution of the selfing syndrome.

Conclusions

We argue that because of its frequent parallel evolution, the selfing syndrome represents an ideal model for addressing basic questions about morphological evolution and adaptation in flowering plants, but that realizing this potential will require the molecular identification of more of the causal genes underlying relevant trait variation.