Clade age and not diversification rate explains species richness among animal taxa

Animal taxa show remarkable variability in species richness across phylogenetic groups. Most explanations for this disparity postulate that taxa with more species have phenotypes or ecologies that cause higher diversification rates (i.e., higher speciation rates or lower extinction rates). Here we show that clade longevity, and not diversification rate, has primarily shaped patterns of species richness across major animal clades: more diverse taxa are older and thus have had more time to accumulate species. Diversification rates calculated from 163 species-level molecular phylogenies were highly consistent within and among three major animal phyla (Arthropoda, Chordata, Mollusca) and did not correlate with species richness. Clades with higher estimated diversification rates were younger, but species numbers increased with increasing clade age. A fossil-based data set also revealed a strong, positive relationship between total extant species richness and crown group age across the orders of insects and vertebrates. These findings do not negate the importance of ecology or phenotype in influencing diversification rates, but they do show that clade longevity is the dominant signal in major animal biodiversity patterns. Thus, some key innovations may have acted through fostering clade longevity and not by heightening diversification rate.     

Genome shrinkage and loss of nutrient-providing potential in the obligate symbiont of the primitive termite Mastotermes darwiniensis

Beneficial microbial associations with insects are common and are classified as either one or a few intracellular species that are vertically transmitted and reside intracellularly within specialized organs or as microbial assemblages in the gut. Cockroaches and termites maintain at least one if not both beneficial associations. Blattabacterium is a flavobacterial endosymbiont of nearly all cockroaches and the termite Mastotermes darwiniensis and can use nitrogenous wastes in essential amino acid and vitamin biosynthesis. Key changes during the evolutionary divergence of termites from cockroaches are loss of Blattabacterium, diet shift to wood, acquisition of a specialized hindgut microbiota, and establishment of advanced social behavior. Termite gut microbes collaborate to fix nitrogen, degrade lignocellulose, and produce nutrients, and the absence of Blattabacterium in nearly all termites suggests that its nutrient-provisioning role has been replaced by gut microbes. M. darwiniensis is a basal, extant termite that solely retains Blattabacterium, which would show evidence of relaxed selection if it is being supplanted by the gut microbiome. This termite-associated Blattabacterium genome is ～8% smaller than cockroach-associated Blattabacterium genomes and lacks genes underlying vitamin and essential amino acid biosynthesis. Furthermore, the M. darwiniensis gut microbiome membership is more consistent between individuals and includes specialized termite gut-associated bacteria, unlike the more variable membership of cockroach gut microbiomes. The M. darwiniensis Blattabacterium genome may reflect relaxed selection for some of its encoded functions, and the loss of this endosymbiont in all remaining termite genera may result from its replacement by a functionally complementary gut microbiota.     

Altricial development in subsocial cockroach ancestors: foundation for the evolution of phenotypic plasticity in termites

SUMMARY Basal termites possess two developmental features that eusocial Hymenoptera lack: the majority of colony members are juveniles whose somatic and reproductive development is temporarily or permanently suspended, and individual development is characterized by extreme phenotypic plasticity. An examination of the literature indicates that the basis for these unique ontogenetic characters is not the prolongation of a pronymphal stage into postembryonic development, as recently suggested. Like other hemimetabolous insects, termites have three embryonic cuticles, and the pronymphal (EC3) cuticle is shed during or shortly after hatch. Nonetheless, a different developmental landmark, dorsal closure, occurs later during embryogenesis in termites than it does in their cockroach relatives, clearly indicating ontogenetic repatterning from an ancestral state. An alternate hypothesis for the origin of isopteran phenotypic plasticity becomes apparent if we remain focused on the phylogenetic and social context of termite evolution. Altricial development occurs in both vertebrate and invertebrate taxa, evolves in response to the parental environment, and is displayed by two distantly related, biparental, wood-feeding cockroaches, including Cryptocercus , the sister-group to termites. It is therefore likely the condition was present in subsocial termite ancestors, and played a complex, multidimensional role in the transition to eusociality. Most relevant to current arguments is that a shift in responsibility for the care of altricial dependents, from parents to the first nutritionally independent nymphs in the family (alloparents), resulted in the developmental stasis of alloparents at a relatively young age. Because early instar cockroaches are not metamorphically competent, these young alloparents would have provided a novel developmental template on which selection could act.     

Death of an order: a comprehensive molecular phylogenetic study confirms that termites are eusocial cockroaches

Termites are instantly recognizable mound-builders and house-eaters: their complex social lifestyles have made them incredibly successful throughout the tropics. Although known as 'white ants', they are not ants and their relationships with other insects remain unclear. Our molecular phylogenetic analyses, the most comprehensive yet attempted, show that termites are social cockroaches, no longer meriting being classified as a separate order (Isoptera) from the cockroaches (Blattodea). Instead, we propose that they should be treated as a family (Termitidae) of cockroaches. It is surprising to find that a group of wood-feeding cockroaches has evolved full sociality, as other ecologically dominant fully social insects (e.g. ants, social bees and social wasps) have evolved from solitary predatory wasps.     

Formyltetrahydrofolate synthetase gene diversity in the guts of higher termites with different diets and lifestyles

In this study, we examine gene diversity for formyl-tetrahydrofolate synthetase (FTHFS), a key enzyme in homoacetogenesis, recovered from the gut microbiota of six species of higher termites. The "higher" termites (family Termitidae), which represent the majority of extant termite species and genera, engage in a broader diversity of feeding and nesting styles than the "lower" termites. Previous studies of termite gut homoacetogenesis have focused on wood-feeding lower termites, from which the preponderance of FTHFS sequences recovered were related to those from acetogenic treponemes. While sequences belonging to this group were present in the guts of all six higher termites examined, treponeme-like FTHFS sequences represented the majority of recovered sequences in only two species (a wood-feeding Nasutitermes sp. and a palm-feeding Microcerotermes sp.). The remaining four termite species analyzed (a Gnathamitermes sp. and two Amitermes spp. that were recovered from subterranean nests with indeterminate feeding strategies and a litter-feeding Rhynchotermes sp.) yielded novel FTHFS clades not observed in lower termites. These termites yielded two distinct clusters of probable purinolytic Firmicutes and a large group of potential homoacetogens related to sequences previously recovered from the guts of omnivorous cockroaches. These findings suggest that the gut environments of different higher termite species may select for different groups of homoacetogens, with some species hosting treponeme-dominated homoacetogen populations similar to those of wood-feeding, lower termites while others host Firmicutes-dominated communities more similar to those of omnivorous cockroaches.     

Fossil evidence for key innovations in the evolution of insect diversity

Explaining the taxonomic richness of the insects, comprising over half of all described species, is a major challenge in evolutionary biology. Previously, several evolutionary novelties (key innovations) have been posited to contribute to that richness, including the insect bauplan, wings, wing folding and complete metamorphosis, but evidence over their relative importance and modes of action is sparse and equivocal. Here, a new dataset on the first and last occurrences of fossil hexapod (insects and close relatives) families is used to show that basal families of winged insects (Palaeoptera, e.g. dragonflies) show higher origination and extinction rates in the fossil record than basal wingless groups (Apterygota, e.g. silverfish). Origination and extinction rates were maintained at levels similar to Palaeoptera in the more derived Polyneoptera (e.g. cockroaches) and Paraneoptera (e.g. true bugs), but extinction rates subsequently reduced in the very rich group of insects with complete metamorphosis (Holometabola, e.g. beetles). Holometabola show evidence of a recent slow-down in their high net diversification rate, whereas other winged taxa continue to diversify at constant but low rates. These data suggest that wings and complete metamorphosis have had the most effect on family-level insect macroevolution, and point to specific mechanisms by which they have influenced insect diversity through time.     

Fossil and phylogenetic analyses reveal recurrent periods of diversification and extinction in dictyopteran insects

Variations of speciation and extinction rates determine the fate of clades through time. Periods of high diversification and extinction (possibly mass-extinction events) can punctuate the evolutionary history of various clades, but they remain loosely defined for many biological groups, especially nonmarine invertebrates like insects. Here, we examine whether the cockroaches, mantises and termites (altogether included in Dictyoptera) have experienced episodic pulses of speciation or extinction and how these pulses may be associated with environmental fluctuations or mass extinctions. We relied on molecular phylogeny and fossil data to shed light on the times and rates at which dictyopterans diversified. The diversification of Dictyoptera has alternated between (i) periods of high diversification in the late Carboniferous, Early–Middle Triassic, Early Cretaceous and middle Palaeogene, and (ii) periods of high extinction rates particularly at the Permian-Triassic boundary, but not necessarily correlated with the major global biodiversity crises as in the mid-Cretaceous. This study advocates the importance of analyzing, when possible, both molecular phylogeny and fossil data to unveil diversification and extinction periods for a given group. The causes and consequences of extinction must be studied beyond mass-extinction events alone to gain a broader understanding of how clades wax and wane.     

Temporal Patterns of Diversification across Global Cichlid Biodiversity (Acanthomorpha: Cichlidae)

The contrasting distribution of species diversity across the major lineages of cichlids makes them an ideal group for investigating macroevolutionary processes. In this study, we investigate whether different rates of diversification may explain the disparity in species richness across cichlid lineages globally. We present the most taxonomically robust time-calibrated hypothesis of cichlid evolutionary relationships to date. We then utilize this temporal framework to investigate whether both species-rich and depauperate lineages are associated with rapid shifts in diversification rates and if exceptional species richness can be explained by clade age alone. A single significant rapid rate shift increase is detected within the evolutionary history of the African subfamily Pseudocrenilabrinae, which includes the haplochromins of the East African Great Lakes. Several lineages from the subfamilies Pseudocrenilabrinae (Australotilapiini, Oreochromini) and Cichlinae (Heroini) exhibit exceptional species richness given their clade age, a net rate of diversification, and relative rates of extinction, indicating that clade age alone is not a sufficient explanation for their increased diversity. Our results indicate that the Neotropical Cichlinae includes lineages that have not experienced a significant rapid burst in diversification when compared to certain African lineages (rift lake). Neotropical cichlids have remained comparatively understudied with regard to macroevolutionary patterns relative to African lineages, and our results indicate that of Neotropical lineages, the tribe Heroini may have an elevated rate of diversification in contrast to other Neotropical cichlids. These findings provide insight into our understanding of the diversification patterns across taxonomically disparate lineages in this diverse clade of freshwater fishes and one of the most species-rich families of vertebrates.     

Evidence from multiple gene sequences indicates that termites evolved from wood-feeding cockroaches

Despite more than half a century of research, the evolutionary origin of termites remains unresolved [1] [2] [3]. A clear picture of termite ancestry is crucial for understanding how these insects evolved eusociality, particularly because they lack the haplodiploid genetic system associated with eusocial evolution in bees, ants, wasps and thrips [4] [5]. Termites, together with cockroaches and praying mantids, constitute the order Dictyoptera, which has been the focus of numerous conflicting phylogenetic studies in recent decades [6] [7] [8] [9] [10] [11] [12]. With the aim of settling the debate over the sister-group of termites, we have determined the sequences of genes encoding 18S ribosomal RNA, mitochondrial cytochrome oxidase subunit II (COII) and endogenous endo-beta-1, 4-glucanase (EG) from a diverse range of dictyopterans. Maximum parsimony and likelihood analyses of these sequences revealed strong support for a clade consisting of termites and subsocial, wood-feeding cockroaches of the genus Cryptocercus. This clade is nested within a larger cockroach clade, implicating wood-feeding cockroaches as an evolutionary intermediate between primitive non-social taxa and eusocial termites.     

Dynamics of host plant use and species diversity in Polygonia butterflies (Nymphalidae)

The ability of insects to utilize different host plants has been suggested to be a dynamic and transient phase. During or after this phase, species can shift to novel host plants or respecialize on ancestral ones. Expanding the range of host plants might also be a factor leading to higher levels of net speciation rates. In this paper, we have studied the possible importance of host plant range for diversification in the genus Polygonia (Nymphalidae, Nymphalini). We have compared species richness between sistergroups in order to find out if there are any differences in number of species between clades including species that utilize only the ancestral host plants ('urticalean rosids') and their sisterclades with a broader (or in some cases potentially broader) host plant repertoire. Four comparisons could be made, and although these are not all phylogenetically or statistically independent, all showed clades including butterfly species using other or additional host plants than the urticalean rosids to be more species-rich than their sisterclade restricted to the ancestral host plants. These results are consistent with the theory that expansions in host plant range are involved in the process of diversification in butterflies and other phytophagous insects, in line with the general theory that plasticity may drive speciation.     

Does host‐plant diversity explain species richness in insects? A test using Coccidae (Hemiptera)

1. The megadiverse herbivores and their host plants are a major component of biodiversity, and their interactions have been hypothesised to drive the diversification of both. 2. If plant diversity influences the diversity of insects, there is an expectation that insect species richness will be strongly correlated with host‐plant species richness. This should be observable at two levels (i) more diverse host‐plant groups should harbour more species of insects, and (ii) the species richness of a group of insects should correlate with the richness of the host groups it uses. However, such a correlation is also consistent with a hypothesis of random host use, in which insects encounter and use hosts in proportion to the diversity of host plants. Neither of these expectations has been widely tested. 3. These expectations were tested using data from a species‐rich group of insects – the Coccidae (Hemiptera). 4. Significant positive correlations were found between the species richness of coccid clades (genera) and the species richness of the host‐plant family or families upon which the clades occur. On a global scale, more closely related plant families have more similar communities of coccid genera but the correlation is weak. 5. Random host use could not be rejected for many coccids but randomisation tests and similarity of coccid communities on closely related plant families show that there is non‐random host use in some taxa. Overall, our results support the idea that plant diversity is a driver of species richness of herbivorous insects, probably via escape‐and‐radiate or oscillation‐type processes.     

The causes of species richness patterns across space, time, and clades and the role of "ecological limits"

A major goal of research in ecology and evolution is to explain why species richness varies across habitats, regions, and clades. Recent reviews have argued that species richness patterns among regions and clades may be explained by "ecological limits" on diversity over time, which are said to offer an alternative explanation to those invoking speciation and extinction (diversification) and time. Further, it has been proposed that this hypothesis is best supported by failure to find a positive relationship between time (e.g., clade age) and species richness. Here, I critically review the evidence for these claims, and propose how we might better study the ecological and evolutionary origins of species richness patterns. In fact, ecological limits can only influence species richness in clades by influencing speciation and extinction, and so this new "alternative paradigm" is simply one facet of the traditional idea that ecology influences diversification. The only direct evidence for strict ecological limits on richness (i.e., constant diversity over time) is from the fossil record, but many studies cited as supporting this pattern do not, and there is evidence for increasing richness over time. Negative evidence for a relationship between clade age and richness among extant clades is not positive evidence for constant diversity over time, and many recent analyses finding no age-diversity relationship were biased to reach this conclusion. More comprehensive analyses strongly support a positive age-richness relationship. There is abundant evidence that both time and ecological influences on diversification rates are important drivers of both large-scale and small-scale species richness patterns. The major challenge for future studies is to understand the ecological and evolutionary mechanisms underpinning the relationships between time, dispersal, diversification, and species richness patterns.     

Cellulose digestion in termites and cockroaches: What role do symbionts play?

• 1.1. Termites and cockroaches are excellent models for studying the role of symbionts in cellulose digestion in insects: they eat cellulose in a variety of forms and may or may not have symbionts.
• 2.2. The wood-eating cockroach, Panesthia cribrata, can be maintained indefinitely, free of microorganisms, on a diet of crystalline cellulose. Under these conditions the RQ is 1, indicating that the cockroach is surviving on glucose produced by endogenous cellulase.
• 3.3. The in vitro rate at which glucose is produced from crystalline cellulose by gut extracts from P. cribrata and Nasutitermes walkeri is comparable to the in vivo production of CO₂ in these insects, clearly indicating that the rate of glucose production from crystalline cellulose is sufficient for their needs.
• 4.4. In all termites and cockroaches examined, cellulase activity was found in the salivary glands and predominantly in the foregut and midgut. These regions are the normal sites of secretion of digestive enzymes and are either devoid of microorganisms (salivary glands) or have very low numbers.
• 5.5. Endogeneous cellulases from termites and cockroaches consist of multiple endo-β-1,4-glucanase (EC 3.2.1.4) and β-1,4-glucosidase (EC 3.2.1.21) components. There is no evidence that an exo-β-1,4-glucanase (cellobiohydrolase) (EC 3.2.1.91) is involved in, or needed for, the production of glucose from crystalline cellulose in termites or cockroaches as the endo-β-1,4-glucanase components are active against both crystalline cellulose and carboxymethylcellulose.
• 6.6. There is no evidence that bacteria are involved in cellulose digestion in termites and cockroaches. The cellulase associated with the fungus garden of M. michaelseni is distinct from that in the midgut; there is little indication that the fungal enzymes are acquired or needed. Lower termites such as Coptotermes lacteus have Protozoa in their hindgut which produce a cellulase(s) quite distinct from that in the foregut and midgut.

     

The fine structure of colleterial glands in two cockroaches and three termites, including a detailed study of Cryptocercus punctulatus (Blattaria, Cryptocercidae) and Mastotermes darwiniensis (Isoptera, Mastotermitidae)

The colleterial glands of insects are organs associated with the female genital apparatus. In cockroaches, these glands produce secretions that cover two parallel rows of eggs during oviposition, and in oviparous species, these secretions become the tanned, sculpted, rigid outer casing of the ootheca. The goal of this study was to compare the gross anatomy of the colleterial glands and the ultrastructure of their component tubules in the phylogenetically significant genera Cryptocercus (Blattaria) and Mastotermes (Isoptera). Recent studies indicate that cockroaches in the genus Cryptocercus are the sister group of termites, and Mastotermes is the only termite known to produce a cockroach-like ootheca. One additional oviparous cockroach, Therea, and two additional termites, Zootermopsis and Pseudacanthotermes, were also examined. As in other cockroaches, the colleterial glands of Cryptocercus and Therea are asymmetrical, with a well developed bipartite left gland and a smaller right gland. In the termites Mastotermes, Zootermopsis, and Pseudacanthotermes, the colleterial glands are composed of a well-developed, paired, anterior gland and a small posterior gland; histological staining and cytological evidence suggest that these are homologues of the left and the right colleterial glands of cockroaches, respectively. At the ultrastructural level, colleterial gland tubules are made of cells belonging to a modified class 1 type cell in the cockroaches, in Mastotermes, and in Zootermopsis; the latter lays its eggs singly, without a surrounding ootheca-like structure. In the advanced termite Pseudacanthotermes, the tubules are made of secretory units belonging to the class 3 cell type. This study demonstrates that the cytological characteristics of colleterial glands in basal termites are similar to those of cockroaches, whether the termite secretes an oothecal casing that covers two parallel rows of eggs, as in Mastotermes, or lays its eggs singly, as in Zootermopsis. The function of colleterial glands in non-mastotermitid termites is unknown.     

IDENTIFICATION OF THE FGL‐AMIDE ALLATOSTATIN GENE OF THE PRIMITIVE TERMITE Mastotermes darwiniensis AND THE WOODROACH Cryptocercus darwini

Allatostatins with the C‐terminal ending Tyr/Phe‐Xaa‐Phe‐Gly‐Leu/Ile‐amide (FGLa/ASTs) are widespread neuropeptides with multiple functions. The gene encoding the FGLa/AST polypeptide precursor was first isolated from cockroaches and since then could be identified in many insects and crustaceans. With its strictly conserved regions in combination with variable regions the gene seems to be a good candidate for phylogenetic analyses between closely and distantly related species. Here, the structure of the FGLa/AST gene of the most primitive termite, the giant northern termite Mastotermes darwiniensis Froggatt, was identified. The FGLa/AST gene of the woodroach Cryptocercus darwini was also determined. Precursor sequences of both species possess the general organization of dictyopteran FGLa/AST precursors containing 14 putative FGLa/AST peptides. In M. darwiniensis, only 11 out of the 14 FGLa/AST‐like peptides possess the C‐terminal conserved region Y/FXFGL/I/V/M and four of the putative peptide structures are not followed by a Gly residue that would lead to nonamidated peptides. Phylogenetic analyses show the high degree of similarity of dictyopteran FGLa/AST sequences. The position of termites, nested within the Blattaria, confirms that termites have evolved from primitive cockroaches.     

Interacting effects of landscape context and habitat quality on flower visiting insects in agricultural landscapes

Landscape context and habitat quality may have pronounced effects on the diversity of flower visiting insects. We investigated whether the effects of landscape context and habitat quality on flower visiting insects interact in agricultural landscapes in the Netherlands. Landscape context was expressed as the area of semi-natural habitats or the density of linear landscape features, and was quantified at spatial scales ranging from 250 to 2000 m. Habitat quality was determined as flower abundance. Species richness and abundance of hoverflies and bees were determined along 16 stream banks experiencing similar environmental conditions but situated in areas with contrasting landscape context. Only flower abundance and the area of semi-natural habitats within 500–1000 m were significantly related to species richness of hoverflies and bees and these factors had interacting effects on both species groups. Our results suggest that the regional area of semi-natural habitats had a positive effect on hoverfly species richness when flower abundance was relatively high, but not when flower abundance was low. Moreover, flower abundance had positive effects on hoverfly species richness only in areas with relatively many semi-natural habitats. Contrastingly, flower abundance had a more positive effect on bee species richness in landscapes with few semi-natural habitats compared to landscapes with more semi-natural habitats. Our results suggest that the importance of landscape context for the species richness of flower visiting insects depends upon the quality of the habitat patches.     

The origin of a 'true' worker caste in termites: mapping the real world on the phylogenetic tree

The evolution of the 'true' worker caste in termites is not decisively inferred by coding and mapping both this character and the foraging behaviour on a phylogenetic tree. Answering to Thompson et al. (2000, 2003), and with reference to Grandcolas and D'Haese (2002), we show that this indecisive inference depends on the correct consideration paid to the outgroups. These last ones could be non subsocial cockroaches, or some wood-eating subsocial cockroaches often considered misleadingly as living ancestors, or even any hemimetabolous insects, all of them would be unambiguously lacking 'true' worker caste and pseudergate caste and not showing the 'one-piece' life type foraging behaviour. These statements derive from observing, coding and mapping the real world on the tree without making ad hoc assumptions. In that respect, because termites do not exist in isolation, apart from the tree of life, mapping the character of interest on the tree must be applied to the outgroups as well.     

Proctolin in the antennal circulatory system of lower Neoptera: a comparative pharmacological and immunohistochemical study

Neuropeptides are important with respect to almost all physiological processes and behavioural patterns in an organism. In the present study, muscle bioassays, immunohistochemistry and matrix‐assisted laser desorption ionization time‐of‐flight (MALDI‐TOF) mass spectrometry are used to investigate the distribution and efficacy of proctolin in the antennal heart of 36 species of lower Neoptera. In total, 20 species of Dictyoptera (cockroaches, termites, praying mantids), eight species of Saltatoria (crickets and grasshoppers) and eight species of Phasmatodea (stick insects) are investigated. The antennal heart of all tested Blattoidea, including the termite Mastotermes darwiniensis Froggatt, exhibit a strong proctolin‐like immunoreactivity, as well as a high sensitivity to proctolin, whereas members of the second clade of cockroaches (Blaberoidea) are largely insensitive to proctolin and show only a weak proctolin‐like immunoreactivity. The antennal heart of praying mantids (Mantodea) also contains only few proctolin‐like immunoreactive fibres but is highly sensitive to proctolin. Such a high sensitivity is found also in Phasmatodea, although the antennal heart of these insects does not have proctolin‐like immunoreactive fibres. These findings are supported by MALDI‐TOF mass spectrometry; no trace of proctolin is detected in antennal heart preparations of Phasmatodea. In Saltatoria, only weak (or no) effects of proctolin are observed and, in most subtaxa, no proctolin‐like immunoreactivity is visible in the antennal heart preparations. Only in Grylloidea is strong proctolin‐like immunostaining found in processes of the antennal heart. In these species, weak or moderate effects of proctolin are observed in the antennal heart bioassay. In general, the differences in distribution of proctolin and effects on the antennal heart within the basal Neoptera cannot be deduced from their phylogenetic position, although they show conformity within each (sub)taxon.