A comparative study of diversification events: the early Paleozoic versus the Mesozoic

We compare two major long-term diversifications of marine animal families that began during periods of low diversity but produced strikingly different numbers of phyla, classes, and orders. The first is the early-Paleozoic diversification (late Vendian-Ordovician; 182 MY duration) and the other the Mesozoic phase of the post-Paleozoic diversification (183 MY duration). The earlier diversification was associated with a great burst of morphological invention producing many phyla, classes, and orders and displaying high per taxon rates of family origination. The later diversification lacked novel morphologies recognized as phyla and classes, produced fewer orders, and displayed lower per taxon rates of family appearances. The chief difference between the diversifications appears to be that the earlier one proceeded from relatively narrow portions of adaptive space, whereas the latter proceeded from species widely scattered among adaptive zones and representing a variety of body plans. This difference is believed to explain the major differences in the products of these great radiations. Our data support those models that hold that evolutionary opportunity is a major factor in the outcome of evolutionary processes.     

Molecular clocks and explosive radiations

Molecular data are ideal for exploring evolutionary history because of its universality, stochasticity, and abundance. These features provide a means of exploring the evolutionary history of all organisms (including those that do not tend to leave fossils), potentially within a statistical framework that allows testing of evolutionary hypotheses. However, the discrepancy between molecular and paleontological dates for three key "explosive" radiations inferred from the fossil record--the Cambrian explosion of animal phyla and the post-KT radiations of modern orders of mammals and birds--have led to a reexamination of the assumptions on which molecular dates are based. Could variation in the rate of molecular evolution, perhaps associated with "explosive" radiations, cause overestimation of diversification dates? Here I examine four hypothetical causes of fast molecular rates in explosive radiations--body size, morphological rate, speciation rate, and ecological diversification--using available empirical evidence on patterns of variation in rate of molecular evolution.     

18S rRNA data indicate that Aschelminthes are polyphyletic in origin and consist of at least three distinct clades

The Aschelminthes is a collection of at least eight animal phyla, historically grouped together because the absence of a true body cavity was perceived as a pseudocoelom. Analyses of 18S rRNA sequences from six Aschelminth phyla (including four previously unpublished sequences) support polyphyly for the Aschelminthes. At least three distinct groups of Aschelminthes were detected: the Priapulida among the protostomes, the Rotifera-Acanthocephala as a sister group to the protostomes, and the Nematoda as a basal group to the triploblastic Eumetazoa.      

Gastrulation.

At gastrulation, a single layer of cells is converted into an outer ectodermal covering, an inner ectodermal tube, and in triploblastic phyla, a middle mesodermal layer. This morphogenesis is driven by motility and directed by cell interactions, some of which involve adhesion and others that involve information transfer.     

A Phylogenetic Analysis of the L1 Family of Neural Cell Adhesion Molecules

L1-type genes form one of several distinct gene families that encode adhesive proteins, which are predominantly expressed in developing and mature metazoan nervous systems. These proteins have a multitude of different important cellular functions in neuronal and glial cells. L1-type gene products are transmembrane proteins with a characteristic extracellular domain structure consisting of six immunoglobulin and three to five fibronectin type III protein folds. As reported here, L1-type proteins can be identified in most metazoan phyla with the notable exception of Porifera (sponges). This puts the origin of L1-type genes at a point in time when primitive cellular neural networks emerged, approximately 1,200 to 1,500 million years ago. Subsequently, several independent gene duplication events generated multiple paralogous L1-type genes in some phyla, allowing for a considerable diversification of L1 structures and the emergence of new functional features and molecular interactions. One such evolutionary newer feature is the appearance of RGD integrin-binding motifs in some vertebrate L1 family members.     

Triploblastic relationships with emphasis on the acoelomates and the position of Gnathostomulida,Cycliophora, Plathelminthes,and Chaetognatha: a combined approach of 18S rDNA sequences and morphology

Triploblastic relationships were examined in the light of molecular and morphological evidence. Representatives for all triploblastic "phyla" (except Loricifera) were represented by both sources of phylogenetic data. The 18S ribosomal (rDNA) sequence data for 145 terminal taxa and 276 morphological characters coded for 36 supraspecific taxa were combined in a total evidence regime to determine the most consistent picture of triploblastic relationships for these data. Only triploblastic taxa are used to avoid rooting with distant outgroups, which seems to happen because of the extreme distance that separates diploblastic from triploblastic taxa according to the 18S rDNA data. Multiple phylogenetic analyses performed with variable analysis parameters yield largely inconsistent results for certain groups such as Chaetognatha, Acoela, and Nemertodermatida. A normalized incongruence length metric is used to assay the relative merit of the multiple analyses. The combined analysis having the least character incongruence yields the following scheme of relationships of four main clades: (1) Deuterostomia [((Echinodermata + Enteropneusta) (Cephalochordata (Urochordata + Vertebrata)))]; (2) Ecdysozoa [(((Priapulida + Kinorhyncha) (Nematoda + Nematomorpha)) ((Onychophora + Tardigrada) Arthropoda))]; (3) Trochozoa [((Phoronida + Brachiopoda) (Entoprocta (Nemertea (Sipuncula (Mollusca (Pogonophora (Echiura + Annelida)))))))]; and (4) Platyzoa [((Gnathostomulida (Cycliophora + Syndermata)) (Gastrotricha + Plathelminthes))]. Chaetognatha, Nemertodermatida, and Bryozoa cannot be assigned to any one of these four groups. For the first time, a data analysis recognizes a clade of acoelomates, the Platyzoa (sensu Cavalier-Smith, Biol. Rev. 73:203-266, 1998). Other relationships that corroborate some morphological analyses are the existence of a clade that groups Gnathostomulida + Syndermata (= Gnathifera), which is expanded to include the enigmatic phylum Cycliophora, as sister group to Syndermata.     

The occurrence of type S1A serine proteases in sponge and jellyfish

Although serine proteases are found in all kinds of cellular organisms and many viruses, the classic "chymotrypsin family" (Group S1A by the 1998 Barrett nomenclature) has an unusual phylogenetic distribution, being especially common in animals, entirely absent from plants and protists, and rare among fungi. The distribution in Bacteria is largely restricted to the genus Streptomyces, although a few isolated occurrences in other bacteria have been reported. The family may be entirely absent from Archaea. Although more than a thousand sequences have been reported for enzymes of this type from animals, none of them have been from early diverging phyla like Porifera or Cnidaria. We now report the existence of Group S1A serine proteases in a sponge (phylum Porifera) and a jellyfish (phylum Cnidaria), making it safe to conclude that all animal groups possess these enzymes.     

The Occurrence of Type S1A Serine Proteases in Sponge and Jellyfish

Although serine proteases are found in all kinds of cellular organisms and many viruses, the classic "chymotrypsin family" (Group S1A by the 1998 Barrett nomenclature) has an unusual phylogenetic distribution, being especially common in animals, entirely absent from plants and protists, and rare among fungi. The distribution in Bacteria is largely restricted to the genus Streptomyces, although a few isolated occurrences in other bacteria have been reported. The family may be entirely absent from Archaea. Although more than a thousand sequences have been reported for enzymes of this type from animals, none of them have been from early diverging phyla like Porifera or Cnidaria. We now report the existence of Group S1A serine proteases in a sponge (phylum Porifera) and a jellyfish (phylum Cnidaria), making it safe to conclude that all animal groups possess these enzymes.     

An analysis of the origin of metazoans, using comparisons of partial sequences of the 28S RNA, reveals an early emergence of triploblasts

In order to study the origin of metazoans, we have compared sequences from the 5' end of the large subunit ribosomal RNA of a number of protists, fungi, plants and metazoans, including all diploblastic phyla (sequences of 10 new species have been determined, including that of the placozoan, Trichoplax adhaerens). These sequences were analyzed using distance matrix, maximum parsimony and maximum likelihood methods, and the validity of the results was ascertained with bootstrapping and species removal or addition. Triploblasts and diploblasts formed two clearly separated monophyletic units; this divergence, which apparently preceded the diversification of diploblastic animals (i.e. the successive sponge, ctenophore, cnidarian radiations), showed a much more ancient origin of triploblasts with respect to diploblasts than classically assumed. These results do not exclude the possibility that triploblasts and diploblasts arose independently from different protists.     

Dynamism and context‐dependency in diversification of the megadiverse plant genus Solanum (Solanaceae)

Explosive radiations—substantial increases in net species diversification—have been considered one of the most intriguing diversification patterns across the Tree of Life, but the subsequent change, movement, and extinction of the constituent lineages make radiations hard to discern or understand as geological time passes. We used the megadiverse angiosperm genus Solanum L. (Solanaceae), with ca. 1200 currently accepted species distributed worldwide in a wide array of habitats, to explore these patterns on a global scale. We synthesized phylogenetic and distributional data for this ongoing radiation to show how dispersal events and past climatic changes have interacted to shape diversification. We find that, despite the vast diversity of Solanum lineages in the Neotropics, lineages in the Old World are diversifying more rapidly. This recent increase in diversification coincides with a long‐distance dispersal event from the Neotropics to regions where major climatic changes were taking place. Two separate groups of Solanum have migrated and established in Australia, but only the arid‐adapted lineages underwent significant increases in diversification rate, as they were able to adapt to the continent's long‐term climatic trend towards seasonally dry and arid biomes (a pattern observed in the diversification of other arid‐adapted groups). Our findings provide a clear example of how successful colonization of new areas and niches can—but does not always—drive explosive diversifications.     

Evolutionary aspects of octopaminergic systems with emphasis on arthropods

We review current knowledge on octopaminergic systems in all major phyla with emphasis on arthropods. Octopaminergic systems occur in all triploblastic animals investigated. Close relationships of the octopamine-receptors in protostomes to vertebrate alpha-adrenergic receptors suggest an ancient common origin. Some evidence suggests that the octopaminergic system may be younger than the vertebrate adrenergic system. All octopaminergic systems are constructed from comparatively few neurons, and the cell populations in different representatives of a given phylum are clearly similar. Current data do not allow any conclusions on the relationships between molluscs and annelids (Lophotrochozoa) to nematodes and arthropods (Ecdysozoa).In chelicerates, including Limulus as a remaining xiphosuran, and crustaceans, octopaminergic neurons occur in pairs. All investigated winged insects (Pterygota) possess similar arrangements of octopaminergic cell populations, suggesting that their octopaminergic systems have been largely conserved during evolution. Unpaired octopaminergic neurons, with symmetrical, bilaterally projecting efferent axons in insects do not appear to have counterparts in other arthropods. Unpaired-octopaminergic neurons may thus be an autapomorphic feature of winged insects. Octopamine acts as an inhibitory neurotransmitter in gastropods, and as an excitatory transmitter controlling bioluminescence in fireflies. Octopamine is also implicated in controlling bioluminescence in other phyla. All critically examined triploblastic invertebrates release octopamine as a hormone, as a peripheral modulator and as a central neuromodulator in the nervous system, which exerts its action via evolutionary related G-protein-coupled receptors that activate cAMP. The evolution of the octopaminergic system seems fundamental for the evolution of efficient locomotory mechanisms, complex social interactions, and cognitive abilities of arthropods.     

Evolutionary relationships of Metazoa within the eukaryotes based on molecular data from Porifera

Recent molecular data provide strong support for the view that all metazoan phyla, including Porifera, are of monophyletic origin. The relationship of Metazoa, including the Porifera, to Plantae, Fungi and unicellular eukaryotes has only rarely been studied by using cDNAs coding for proteins. Sequence data from rDNA suggested a relationship of Porifera to unicellular eukaryotes (choanoflagellates). However, ultrastructural studies of choanocytes did not support these findings. In the present study, we compared amino acid sequences that are found in a variety of metazoans (including sponges) with those of Plantae, Fungi and unicellular eukaryotes, to obtain an answer to this question. We used the four sequences from 70 kDa heat-shock proteins, the serine-threonine kinase domain found in protein kinases, beta-tubulin and calmodulin. The latter two sequences were deduced from cDNAs, isolated from the sponge Geodia cydonium for the phylogenetic analyses presented. These revealed that the sponge molecules were grouped into the same branch as the Metazoa, which is statistically (significantly) separated from those branches that comprise the sequences from Fungi, Plantae and unicellular eukaryotes. From our molecular data it seems evident that the unicellular eukaryotes existed at an earlier stage of evolution, and the Plantae and especially the Fungi and the Metazoa only appeared later.     

T-box and homeobox genes from the ctenophore Pleurobrachia pileus: comparison of Brachyury, Tbx2/3 and Tlx in basal metazoans and bilaterians

Most animals are classified as Bilateria and only four phyla are still extant as outgroups, namely Porifera, Placozoa, Cnidaria and Ctenophora. These non-bilaterians were not considered to have a mesoderm and hence mesoderm-specific genes. However, the T-box gene Brachyury could be isolated from sponges, placozoans and cnidarians. Here, we describe the first Brachyury and a Tbx2/3 homologue from a ctenophore. In addition, analysing T-box and homeobox genes under comparable conditions in all four basal phyla lead to the discovery of novel T-box genes in sponges and cnidarians and a Tlx homeobox gene in the ctenophore Pleurobrachia pileus. The conservation of the T-box and the homeobox genes suggest that distinct subfamilies with different roles in bilaterians were already split in non-bilaterians.     

Spatiotemporal Evolution of the Global Species Diversity of Rhododendron

Evolutionary radiation is a widely recognized mode of species diversification, but its underlying mechanisms have not been unambiguously resolved for species-rich cosmopolitan plant genera. In particular, it remains largely unknown how biological and environmental factors have jointly driven its occurrence in specific regions. Here, we use Rhododendron, the largest genus of woody plants in the Northern Hemisphere, to investigate how geographic and climatic factors, as well as functional traits, worked together to trigger plant evolutionary radiations and shape the global patterns of species richness based on a solid species phylogeny. Using 3,437 orthologous nuclear genes, we reconstructed the first highly supported and dated backbone phylogeny of Rhododendron comprising 200 species that represent all subgenera, sections, and nearly all multispecies subsections, and found that most extant species originated by evolutionary radiations when the genus migrated southward from circumboreal areas to tropical/subtropical mountains, showing rapid increases of both net diversification rate and evolutionary rate of environmental factors in the Miocene. We also found that the geographically uneven diversification of Rhododendron led to a much higher diversity in Asia than in other continents, which was mainly driven by two environmental variables, that is, elevation range and annual precipitation, and were further strengthened by the adaptation of leaf functional traits. Our study provides a good example of integrating phylogenomic and ecological analyses in deciphering the mechanisms of plant evolutionary radiations, and sheds new light on how the intensification of the Asian monsoon has driven evolutionary radiations in large plant genera of the Himalaya-Hengduan Mountains.     

What can DNA Tell us About the Cambrian Explosion?

Molecular data is ideal for exploring deep evolutionary historybecause of its universality, stochasticity and abundance. Thesefeatures provide a means of exploring the evolutionary historyof all organisms (including those that do not tend to leavefossils), independently of morphological evolution, and withina statistical framework that allows testing of evolutionaryhypotheses. In particular, molecular data have an importantrole to play in examining hypotheses concerning the tempo andmode of evolution of animal body plans. Examples are given wheremolecular phylogenies have led to a re-examination of some fundamentalassumptions in metazoan evolution, such as the immutabilityof early developmental characters, and the evolvability of bauplancharacters. Molecular data is also providing a new and controversialtimescale for the evolution of animal phyla, pushing the majordivisions of the animal kingdom deep into the Precambrian. Therehave been many reasons to question the accuracy and precisionof molecular date estimates, such as the failure to accountfor lineage-specific rate variation and unreliable estimationof rates of molecular evolution. While these criticisms havebeen largely countered by recent studies, one problem has remaineda challenge: could temporal variation in the rate of molecularevolution, perhaps associated with "explosive" adaptive radiations,cause overestimation of diversification dates? Empirical evidencefor an effect of speciation rate, morphological evolution orecological diversification on rates of molecular evolution isexamined, and the potential for rate-variable methods for moleculardating are discussed.     

Ancient lakes revisited: from the ecology to the genetics of speciation

Explosive speciation in ancient lakes has fascinated biologists for centuries and has inspired classical work on the tempo and modes of speciation. Considerable attention has been directed towards the extrinsic forces of speciation—the geological, geographical and ecological peculiarities of ancient lakes. Recently, there has been a resurgence of interest in the intrinsic nature of these radiations, the biological characteristics conducive to speciation. While new species are thought to arise mainly by the gradual enhancement of reproductive isolation among geographically isolated populations, ancient lakes provide little evidence for a predominant role of geography in speciation. Recent phylogenetic work provides strong evidence that multiple colonization waves were followed by parallel intralacustrine radiations that proceeded at relatively rapid rates despite long‐term gene flow through hybridization and introgression. Several studies suggest that hybridization itself might act as a key evolutionary mechanism by triggering major genomic reorganization/revolution and enabling the colonization of new ecological niches in ancient lakes. These studies propose that hybridization is not only of little impediment to diversification but could act as an important force in facilitating habitat transitions, promoting postcolonization adaptations and accelerating diversification. Emerging ecological genomic approaches are beginning to shed light on the long‐standing evolutionary dilemma of speciation in the face of gene flow. We propose an integrative programme for future studies on speciation in ancient lakes.     

Trophic novelty is linked to exceptional rates of morphological diversification in two adaptive radiations of Cyprinodon pupfish

Adaptive radiations are known for rapid morphological and species diversification in response to ecological opportunity, but it remains unclear if distinct mechanisms drive this pattern. Here, we show that rapid rates of morphological diversification are linked to the evolution of novel ecological niches in two independent Cyprinodon radiations nested within a wide-ranging group repeatedly isolated in extreme environments. We constructed a molecular phylogeny for the Cyprinodontidae, measured 16 functional traits across this group, and compared the likelihoods of single or multiple rates of morphological diversification. We found that rates of morphological diversification within two sympatric Cyprinodon clades containing unique trophic specialists are not part of an adaptive continuum with other clades, but are instead extreme outliers with rates up to 131 times faster than other Cyprinodontidae. High rates were not explained by clade age, but were instead linked to unique trophic niches within Cyprinodon, including scale-eating, zooplanktivory, and piscivory. Furthermore, although both radiations occur in similar environments and have similar sister species, they each evolved unique trophic specialists and high rates of morphological diversification in different sets of traits. We propose that the invasion of novel ecological niches may be a key mechanism driving many classic examples of adaptive radiation.     

The distribution of species diversity across a flora's component lineages: dating the Cape's 'relicts'

The Cape Floristic Region is exceptionally species-rich both for its area and latitude, and this diversity is highly unevenly distributed among genera. The modern flora is hypothesized to result largely from recent (post-Oligocene) speciation, and it has long been speculated that particular species-poor lineages pre-date this burst of speciation. Here, we employ molecular phylogenetic data in combination with fossil calibrations to estimate the minimum duration of Cape occupation by 14 unrelated putative relicts. Estimates vary widely between lineages (7-101 Myr ago), and when compared with the estimated timing of onset of the modern flora's radiation, it is clear that many, but possibly not all, of these lineages pre-date its establishment. Statistical comparisons of diversities with lineage age show that low species diversity of many of the putative relicts results from a lower rate of diversification than in dated Cape radiations. In other putative relicts, however, we cannot reject the possibility that they diversify at the same underlying rate as the radiations, but have been present in the Cape for insufficient time to accumulate higher diversity. Although the extremes in diversity of currently dated Cape lineages fall outside expectations under a constant underlying diversification rate, sampling of all Cape lineages would be required to reject this null hypothesis.     

Temporal patterns of diversification in Andean Eois, a species-rich clade of moths (Lepidoptera, Geometridae)

The timing of the origin of present day Neotropical animal diversity is still a matter of debate. For a long time, a preponderance of glacial (i.e. Pleistocene) radiations has been proposed. However, recent data from molecular clock studies indicate a preglacial origin for most of the examined taxa. We performed a fossil-calibrated molecular dating analysis of the genus Eois, which is a major component of one of the world's most diverse assemblages of herbivorous insects. We found that diversification of Eois took place in the Miocene following a pattern best explained by density-dependent diversification. A strong slowdown of diversification towards the present was detected. Diversification of Eois does overlap with increased Andean uplift and diversification of the most commonly used host plant genus Piper. These findings match the patterns found for the majority of Neotropical tetrapods and for three other unrelated, ecologically different lepidopteran genera.     

Phylogenetic Patterns of Geographical and Ecological Diversification in the Subgenus Drosophila

Colonisation of new geographic regions and/or of new ecological resources can result in rapid species diversification into the new ecological niches available. Members of the subgenus Drosophila are distributed across the globe and show a large diversity of ecological niches. Furthermore, taxonomic classification of Drosophila includes the rank radiation, which refers to closely related species groups. Nevertheless, it has never been tested if these taxonomic radiations correspond to evolutionary radiations. Here we present a study of the patterns of diversification of Drosophila to test for increased diversification rates in relation to the geographic and ecological diversification processes. For this, we have estimated and dated a phylogeny of 218 species belonging to the major species groups of the subgenus. The obtained phylogenies are largely consistent with previous studies and indicate that the major groups appeared during the Oligocene/Miocene transition or early Miocene, characterized by a trend of climate warming with brief periods of glaciation. Ancestral reconstruction of geographic ranges and ecological resource use suggest at least two dispersals to the Neotropics from the ancestral Asiatic tropical disribution, and several transitions to specialized ecological resource use (mycophagous and cactophilic). Colonisation of new geographic regions and/or of new ecological resources can result in rapid species diversification into the new ecological niches available. However, diversification analyses show no significant support for adaptive radiations as a result of geographic dispersal or ecological resource shift. Also, cactophily has not resulted in an increase in the diversification rate of the repleta and related groups. It is thus concluded that the taxonomic radiations do not correspond to adaptive radiations.