Ancestral Trait Research Articles

Phylogenetic Comparative Methods on Phylogenetic Networks with Reticulations.

The goal of phylogenetic comparative methods (PCMs) is to study the distribution of quantitative traits among related species. The observed traits are often seen as the result of a Brownian Motion (BM) along the branches of a phylogenetic tree. Reticulation events such as hybridization, gene flow or horizontal gene transfer, can substantially affect a species' traits, but are not modeled by a tree. Phylogenetic networks have been designed to represent reticulate evolution. As they become available for downstream analyses, new models of trait evolution are needed, applicable to networks. We develop here an efficient recursive algorithm to compute the phylogenetic variance matrix of a trait on a network, in only one preorder traversal of the network. We then extend the standard PCM tools to this new framework, including phylogenetic regression with covariates (or phylogenetic ANOVA), ancestral trait reconstruction, and Pagel's $\lambda$ test of phylogenetic signal. The trait of a hybrid is sometimes outside of the range of its two parents, for instance because of hybrid vigor or hybrid depression. These two phenomena are rather commonly observed in present-day hybrids. Transgressive evolution can be modeled as a shift in the trait value following a reticulation point. We develop a general framework to handle such shifts and take advantage of the phylogenetic regression view of the problem to design statistical tests for ancestral transgressive evolution in the evolutionary history of a group of species. We study the power of these tests in several scenarios and show that recent events have indeed the strongest impact on the trait distribution of present-day taxa. We apply those methods to a data set of Xiphophorus fishes, to confirm and complete previous analysis in this group. All the methods developed here are available in the Julia package PhyloNetworks.

Renewed classification within Goniurosaurus (Squamata: Eublepharidae) uncovers the dual roles of a continental island (Hainan) in species evolution

Continental islands are often dynamic in regard to the origin and evolution of their biota. Although colonizations from mainland Southeast Asia to Hainan Island have been reported, the role of Hainan Island as a source for continental biota has not been considered. Goniurosaurus is a genus comprised of nocturnal ground geckos. We reexamined the evolutionary history of Goniurosaurus using both molecular phylogenetics and morphological comparisons. All phylogenetic trees recovered G. zhoui as sister to G. hainanensis + G. lichtenfelderi, which together are the sister lineage of G. bawanglingensis. The recovery of this “Hainan clade” contradicts previous classifications that placed G. bawanglingensis within the G. luii group. Moreover, ancestral trait reconstruction revealed that body band number might have decreased two or three times independently within Goniurosaurus from four to three. The divergence between the continental G. luii group and the Hainan clade was estimated at ∼34.7 Mya (CI = 22.3–48.6), possibly correlating with the vicariance event between Hainan Island and the mainland. G. lichtenfelderi diverged from G. hainanensis very recently, which might be associated with a historical dispersal event from Hainan Island to Vietnam during glacial periods. Our study improves the understanding of Goniurosaurus systematics and reveals the important role of Hainan Island in bidirectional colonizations.

Genome Size, Molecular Phylogeny, and Evolutionary History of the Tribe Aquilarieae (Thymelaeaceae), the Natural Source of Agarwood.

The tribe Aquilarieae of the family Thymelaeaceae consists of two genera, Aquilaria and Gyrinops, with a total of 30 species, distributed from northeast India, through southeast Asia and the south of China, to Papua New Guinea. They are an important botanical resource for fragrant agarwood, a prized product derived from injured or infected stems of these species. The aim of this study was to estimate the genome size of selected Aquilaria species and comprehend the evolutionary history of Aquilarieae speciation through molecular phylogeny. Five non-coding chloroplast DNA regions and a nuclear region were sequenced from 12 Aquilaria and three Gyrinops species. Phylogenetic trees constructed using combined chloroplast DNA sequences revealed relationships of the studied 15 members in Aquilarieae, while nuclear ribosomal DNA internal transcribed spacer (ITS) sequences showed a paraphyletic relationship between Aquilaria species from Indochina and Malesian. We exposed, for the first time, the estimated divergence time for Aquilarieae speciation, which was speculated to happen during the Miocene Epoch. The ancestral split and biogeographic pattern of studied species were discussed. Results showed no large variation in the 2C-values for the five Aquilaria species (1.35–2.23 pg). Further investigation into the genome size may provide additional information regarding ancestral traits and its evolution history.

A Comparative View on Sex Differentiation and Gametogenesis Genes in Lungfish and Coelacanths.

Gonadal sex differentiation and reproduction are the keys to the perpetuation of favorable gene combinations and positively selected traits. In vertebrates, several gonad development features that differentiate tetrapods and fishes are likely to be, at least in part, related to the water-to-land transition. The collection of information from basal sarcopterygians, coelacanths, and lungfishes, is crucial to improve our understanding of the molecular evolution of pathways involved in reproductive functions, since these organisms are generally regarded as “living fossils” and as the direct ancestors of tetrapods. Here, we report for the first time the characterization of >50 genes related to sex differentiation and gametogenesis in Latimeria menadoensis and Protopterus annectens. Although the expression profiles of most genes is consistent with the intermediate position of basal sarcopterygians between actinopterygian fish and tetrapods, their phylogenetic placement and presence/absence patterns often reveal a closer affinity to the tetrapod orthologs. On the other hand, particular genes, for example, the male gonad factor gsdf (Gonadal Soma-Derived Factor), provide examples of ancestral traits shared with actinopterygians, which disappeared in the tetrapod lineage.

Evidence for convergent evolution of host parasitic manipulation in response to environmental conditions.

Environmental conditions exert strong selection on animal behavior. We tested the hypothesis that the altered behavior of hosts due to parasitic manipulation is also subject to selection imposed by changes in environmental conditions over time. Our model system is ants manipulated by parasitic fungi to bite onto vegetation. We analyzed the correlation between forest type (tropical vs. temperate) and the substrate where the host bites (biting substrate: leaf vs. twigs), the time required for the fungi to reach reproductive maturity, and the phylogenetic relationship among specimens from tropical and temperate forests from different parts of the globe. We show that fungal development in temperate forests is longer than the period of time leaves are present and the ants are manipulated to bite twigs. When biting twigs, 90% of the dead ants we examined had their legs wrapped around twigs, which appears to provide better attachment to the plant. Ancestral state character reconstruction suggests that leaf biting is the ancestral trait and that twig biting is a convergent trait in temperate regions of the globe. These three lines of evidence suggest that changes in environmental conditions have shaped the manipulative behavior of the host by its parasite.

Horizontal operon transfer, plasmids, and the evolution of photosynthesis in Rhodobacteraceae

The capacity for anoxygenic photosynthesis is scattered throughout the phylogeny of the Proteobacteria. Their photosynthesis genes are typically located in a so-called photosynthesis gene cluster (PGC). It is unclear (i) whether phototrophy is an ancestral trait that was frequently lost or (ii) whether it was acquired later by horizontal gene transfer. We investigated the evolution of phototrophy in 105 genome-sequenced Rhodobacteraceae and provide the first unequivocal evidence for the horizontal transfer of the PGC. The 33 concatenated core genes of the PGC formed a robust phylogenetic tree and the comparison with single-gene trees demonstrated the dominance of joint evolution. The PGC tree is, however, largely incongruent with the species tree and at least seven transfers of the PGC are required to reconcile both phylogenies. The origin of a derived branch containing the PGC of the model organism Rhodobacter capsulatus correlates with a diagnostic gene replacement of pufC by pufX. The PGC is located on plasmids in six of the analyzed genomes and its DnaA-like replication module was discovered at a conserved central position of the PGC. A scenario of plasmid-borne horizontal transfer of the PGC and its reintegration into the chromosome could explain the current distribution of phototrophy in Rhodobacteraceae.

Developmental changes in song production in free-living male and female New Zealand bellbirds

Song development research has been dominated by studies of northern hemisphere species where typically only males sing. However, female song is present in many species and recent research shows that female song is in fact the ancestral trait for songbirds. Here we present results from a field-based cross-sectional study comparing song development in both sexes of New Zealand bellbirds, Anthornis melanura. We asked whether both sexes develop song at a similar rate, and how the components of a song differ with age. The motor phases of each sex began at similar ages, with subsong starting at 3 weeks posthatching and song types crystallizing by 24 weeks. Song components were compared between three age groups: learning phase, first breeding season and adults. Song structure and acoustic properties were similar between sexes within the learning phase (except for mean fundamental frequency) but differed in adults. The variety of syllable types produced was more widespread in the learning phase and differed significantly between age groups and sexes. Individual syllable production varied in consistency between age groups for both sexes and we suggest that more complex syllables may require more practice to develop to maturity. The findings support the consensus that female and male bellbirds learn song at similar rates; however, differences between the sexes in the learned song components result in sexually dimorphic songs. This study is novel in that we used a field-based approach in which the complex song of male and female wild birds was compared between age groups ranging from fledging to adulthood. Our study contributes to current knowledge of female song development, a topic important for further understanding the selection pressures driving song evolution in songbirds.

Multicopy plasmids allow bacteria to escape from fitness trade-offs during evolutionary innovation.

Understanding the mechanisms governing innovation is a central element of evolutionary theory. Novel traits usually arise through mutations in existing genes, but trade-offs between new and ancestral protein functions are pervasive and constrain the evolution of innovation. Classical models posit that evolutionary innovation circumvents the constraints imposed by trade-offs through genetic amplifications, which provide functional redundancy. Bacterial multicopy plasmids provide a paradigmatic example of genetic amplification, yet their role in evolutionary innovation remains largely unexplored. Here, we reconstructed the evolution of a new trait encoded in a multicopy plasmid using TEM-1 β-lactamase as a model system. Through a combination of theory and experimentation, we show that multicopy plasmids promote the coexistence of ancestral and novel traits for dozens of generations, allowing bacteria to escape the evolutionary constraints imposed by trade-offs. Our results suggest that multicopy plasmids are excellent platforms for evolutionary innovation, contributing to explain their extreme abundance in bacteria.

Notes on maternal behaviour in soft ticks: Specifically observed in Argas (Argas) striatus Bedford, 1932 and Argas (Secretargas) transgariepinus White, 1846

Maternal behaviour (carrying of larvae on the opisthosoma) in ticks has thus far only been observed in Antricola (Parantricola) marginatus and was considered a unique derived adaptation of this genus. The authors extend this observation to two additional argasid species, namely Argas (Argas) striatus and Argas (Secretargas) transgariepinus. In addition, brooding behaviour over eggs were observed with A. (S.) transgariepinus. Maternal behaviour may be an evolutionary adaptation to ecological challenges in habitats unsuited for larval survival and may be related to the presence of pulvilli in larvae. This adaptation might have been present in the ancestral tick lineage since pulvilli occur in all tick families, and may have been derived from a more ancient adaptation in chelicerates where maternal behaviour was common. Female A. (S.) transgariepinus also possess a unique area on their ventral abdomen that is absent in males and may be a unique adaptation for maternal behaviour in this species. Phylogenetic analysis of the 16S rRNA genes for both species indicate that they are unique lineages that group basal to other members of the Argas genus, supporting the possibility that they harbour ancestral traits for this group.

Acquisition of a Novel Sulfur-Oxidizing Symbiont in the Gutless Marine Worm Inanidrilus exumae.

ABSTRACTGutless phallodrilines are marine annelid worms without a mouth or gut, which live in an obligate association with multiple bacterial endosymbionts that supply them with nutrition. In this study, we discovered an unusual symbiont community in the gutless phallodriline Inanidrilus exumae that differs markedly from the microbiomes of all 22 of the other host species examined. Comparative 16S rRNA gene sequence analysis and fluorescence in situ hybridization revealed that I. exumae harbors cooccurring gamma-, alpha-, and deltaproteobacterial symbionts, while all other known host species harbor gamma- and either alpha- or deltaproteobacterial symbionts. Surprisingly, the primary chemoautotrophic sulfur oxidizer “Candidatus Thiosymbion” that occurs in all other gutless phallodriline hosts does not appear to be present in I. exumae. Instead, I. exumae harbors a bacterial endosymbiont that resembles “Ca. Thiosymbion” morphologically and metabolically but originates from a novel lineage within the class Gammaproteobacteria. This endosymbiont, named Gamma 4 symbiont here, had a 16S rRNA gene sequence that differed by at least 7% from those of other free-living and symbiotic bacteria and by 10% from that of “Ca. Thiosymbion.” Sulfur globules in the Gamma 4 symbiont cells, as well as the presence of genes characteristic for autotrophy (cbbL) and sulfur oxidation (aprA), indicate that this symbiont is a chemoautotrophic sulfur oxidizer. Our results suggest that a novel lineage of free-living bacteria was able to establish a stable and specific association with I. exumae and appears to have displaced the “Ca. Thiosymbion” symbionts originally associated with these hosts.IMPORTANCE All 22 gutless marine phallodriline species examined to date live in a highly specific association with endosymbiotic, chemoautotrophic sulfur oxidizers called “Ca. Thiosymbion.” These symbionts evolved from a single common ancestor and represent the ancestral trait for this host group. They are transmitted vertically and assumed to be in transition to becoming obligate endosymbionts. It is therefore surprising that despite this ancient, evolutionary relationship between phallodriline hosts and “Ca. Thiosymbion,” these symbionts are apparently no longer present in Inanidrilus exumae. They appear to have been displaced by a novel lineage of sulfur-oxidizing bacteria only very distantly related to “Ca. Thiosymbion.” Thus, this study highlights the remarkable plasticity of both animals and bacteria in establishing beneficial associations: the phallodriline hosts were able to acquire and maintain symbionts from two very different lineages of bacteria, while sulfur-oxidizing bacteria from two very distantly related lineages were able to independently establish symbiotic relationships with phallodriline hosts.

Morphology and ontogeny of Lophopus crystallinus lophophore support the epistome as ancestral character of phylactolaemate bryozoans

Phylactolaemate bryozoans are the sister-group to all remaining bryozoan taxa. Consequently, their study is essential to reveal and analyze ancestral traits of Phylactolaemata and Bryozoa in general. They are the only bryozoans to possess an epistome which traditionally has been regarded as shared with phoronids and brachiopods. Contrary to older observations, an epistome was recently reported to be missing in the early branching phylactolaemate Lophopus crystallinus. In this study, the ontogeny of the lophophoral base and also its three-dimensional structure in adult specimens was reinvestigated to assess whether an epistome is never formed during ontogeny and absent in adult specimens. The results show that organogenesis during the budding process in this species is similar to other, previously investigated, species. The epistome anlage in L. crystallinus forms in early buds from the outer budding layer which penetrates the two shanks of the u-shaped gut. This ingression of the epithelium further proceeds distally and starts to wrap over the forming ganglion. The adult epistome is a rather short, but present bulge above the cerebral ganglion with prominent muscle bundles traversing its cavity. Distally it is arched by the forked canal that in L. crystallinus has a particularly thick and prominent epithelium in the three median tentacles. This study shows that neither during ontogeny nor in the adult stage an epistome is absent. The epistome is less pronounced than in other phylactolaemates, but otherwise similar in its general structure. Consequently, an epistome can be assumed to be present in the ground pattern of Phylactolaemata.

Factors driving metabolic diversity in the budding yeast subphylum

BackgroundAssociations between traits are prevalent in nature, occurring across a diverse range of taxa and traits. Individual traits may co-evolve with one other, and these correlations can be driven by factors intrinsic or extrinsic to an organism. However, few studies, especially in microbes, have simultaneously investigated both across a broad taxonomic range. Here we quantify pairwise associations among 48 traits across 784 diverse yeast species of the ancient budding yeast subphylum Saccharomycotina, assessing the effects of phylogenetic history, genetics, and ecology.ResultsWe find extensive negative (traits that tend to not occur together) and positive (traits that tend to co-occur) pairwise associations among traits, as well as between traits and environments. These associations can largely be explained by the biological properties of the traits, such as overlapping biochemical pathways. The isolation environments of the yeasts explain a minor but significant component of the variance, while phylogeny (the retention of ancestral traits in descendant species) plays an even more limited role. Positive correlations are pervasive among carbon utilization traits and track with chemical structures (e.g., glucosides and sugar alcohols) and metabolic pathways, suggesting a molecular basis for the presence of suites of traits. In several cases, characterized genes from model organisms suggest that enzyme promiscuity and overlapping biochemical pathways are likely mechanisms to explain these macroevolutionary trends. Interestingly, fermentation traits are negatively correlated with the utilization of pentose sugars, which are major components of the plant biomass degraded by fungi and present major bottlenecks to the production of cellulosic biofuels. Finally, we show that mammalian pathogenic and commensal yeasts have a suite of traits that includes growth at high temperature and, surprisingly, the utilization of a narrowed panel of carbon sources.ConclusionsThese results demonstrate how both intrinsic physiological factors and extrinsic ecological factors drive the distribution of traits present in diverse organisms across macroevolutionary timescales.

A biogeographic perspective on the evolution of fire syndromes in pine trees (Pinus: Pinaceae).

Our goals were to explore the relationship between biogeography and the evolution of fire-adaptive syndromes in the genus Pinus. We used a previously published time-calibrated phylogeny and conducted ancestral trait reconstruction to estimate the likely timing of diversification in Pinus, and to determine when fire-adaptive syndromes evolved in the lineage. To explore trait conservation among fire syndromes and to investigate historical biogeography, we constructed ancestral state reconstructions using the program RASP and estimated the degree of conservatism for fire-adapted traits in the program BaTS. Our reconstructions suggest that the Bering land bridge, which connected North America and Asia, probably played a major role in early pine evolution. Our estimates indicated that fire-adaptive syndromes seem to have evolved more frequently in New World taxa and probably are related to the uplift of major North American mountain ranges. Our data suggest that certain geographically widespread adaptations to fire evolved repeatedly, possibly due to localized changes in climate and environment, rather than resulting from large dispersal events of pre-adapted individuals.

Macronutrient composition of milk of captive nine-banded armadillos (Dasypus novemcinctus)

Armadillo pups rapidly grow a bony carapace, suggesting a large transfer of calcium and phosphorus from mother to pups via milk. Because Ca and P in milk are bound in casein protein micelles, we predicted armadillo milk to be high in protein content. Milk samples (n = 25) from 10 lactating nine-banded armadillos (Dasypus novemcinctus) collected at days 1–6, 14–15, 33–38, and 49–51 after birth were assayed for macronutrient composition (water, fat, protein, sugar, ash, Ca, and P). Gross energy (GE) was calculated from protein, sugar, and fat. Protein concentration (8–11%) was the highest of the milk solids at all time points, and ash (total mineral) values increased from 1.6% to 3.6% and were higher than sugar values (2.4%) after 1 month. Calcium concentration increased from 0.4% to over 1.0% by 1 month of lactation. Calcium and phosphorus were strongly correlated with milk protein (r = 0.796 and 0.815, respectively; P < 0.001). Protein contributed the majority of milk GE over the first 2 weeks of lactation (51%) and was equal to fat after 1 month (both about 47% of GE). The proportion of GE from sugar declined from 14.5% to 6.6%. We suggest that a milk high in protein was an ancestral trait for armadillos that allowed the evolution of a bony carapace by enabling large amounts of Ca and P to be transferred via casein micelles. Based on data from giant anteater (Myrmecophaga tridactyla) milk, a highprotein milk may be ancestral to all Xenarthrans, but this suggestion awaits confirmation from data on the milk of sloths. We suggest that armadillo pups likely catabolize a significant amount of milk protein for metabolic energy.

Diversity of pollination ecology in the Schismatoglottis Calyptrata Complex Clade (Araceae).

Field studies integrating pollination investigations with an assessment of floral scent composition and thermogenesis in tropical aroids are rather few. Thus, this study aimed to investigate the pollination biology of nine species belonging to Schismatoglottis Calyptrata Complex Clade. The flowering mechanism, visiting insect activities, reproductive system, thermogenesis and floral scent composition were examined. Anthesis for all species started at dawn and lasted 25-29h. Colocasiomyia (Diptera, Drosophilidae) are considered the main pollinators for all the investigated species. Cycreon (Coleoptera, Hydrophilidae) are considered secondary pollinators as they are only present in seven of the nine host plants, despite the fact that they are the most effective pollen carrier, carrying up to 15 times more pollen grains than Colocasiomyia flies. However, the number of Colocasiomyia individuals was six times higher than Cycreon beetles. Chaloenus (Chrysomelidae, Galeuricinae) appeared to be an inadvertent pollinator. Atheta (Coleoptera, Staphylinidae) is considered a floral visitor in most investigated species of the Calyptrata Complex Clade in Sarawak, but a possible pollinator in S.muluensis. Chironomidae midges and pteromalid wasps are considered visitors in S.calyptrata. Thermogenesis in a biphasic pattern was observed in inflorescences of S.adducta, S.calyptrata, S.giamensis, S.pseudoniahensis and S.roh. The first peak occurred during pistillate anthesis; the second peak during staminate anthesis. Inflorescences of all investigated species of Calyptrata Complex Clade emitted four types of ester compound, with methyl ester-3-methyl-3-butenoic acid as a single major VOC (volatile organic compound). The appendix, pistillate zone, staminate zone and spathe emitted all these compounds. A mixed fly-beetle pollination system is considered an ancestral trait in the Calyptrata Complex Clade, persisting in Sarawak taxa, whereas the marked reduction of interpistillar staminodes in taxa from Peninsular Malaysia and especially, Ambon, Indonesia, is probably linked to a shift in these taxa to a fly-pollinated system.

Phylogeny and salt-tolerance of freshwater Nostocales strains: Contribution to their systematics and evolution

Phylogenetic relationships among heterocytous genera (the Nostocales order) have been profoundly modified since the use of polyphasic approaches that include molecular data. There is nonetheless still ample scope for improving phylogenetic delineations of genera with broad ecological distributions, particularly by integrating specimens from specific or up-to-now poorly sampled habitats. In this context, we studied 36 new isolates belonging to Chrysosporum, Dolichospermum, Anabaena, Anabaenopsis, and Cylindrospermopsis from freshwater ecosystems of Burkina-Faso, Senegal, and Mayotte Island. Studying strains from these habitats is of particular interest as we suspected different range of salt variations during underwent periods of drought in small ponds and lakes. Such salt variation may cause different adaptation to salinity. We then undertook a polyphasic approach, combining molecular phylogenies, morphological analyses, and physiological measurements of tolerance to salinity. Molecular phylogenies of 117 Nostocales sequences showed that the 36 studied strains were distributed in seven lineages: Dolichospermum, Chrysosporum, Cylindrospermopsis/Raphidiopsis, Anabaenopsis, Anabaena sphaerica var tenuis/Sphaerospermopsis, and two independent Anabaena sphaerica lineages. Physiological data were congruent with molecular results supporting the separation into seven lineages. In an evolutionary context, salinity tolerance can be used as an integrative marker to reinforce the delineation of some cyanobacterial lineages. The history of this physiological trait contributes to a better understanding of processes leading to the divergence of cyanobacteria. In this study, most of the cyanobacterial strains isolated from freshwater environments were salt-tolerant, thus suggesting this trait constituted an ancestral trait of the heterocytous cyanobacteria and that it was probably lost two times secondarily and independently in the ancestor of Dolichospermum and of Cylindrospermopsis.

The invasive MED/Q Bemisia tabaci genome: a tale of gene loss and gene gain

BackgroundSweetpotato whitefly, Bemisia tabaci MED/Q and MEAM1/B, are two economically important invasive species that cause considerable damages to agriculture crops through direct feeding and indirect vectoring of plant pathogens. Recently, a draft genome of B. tabaci MED/Q has been assembled. In this study, we focus on the genomic comparison between MED/Q and MEAM1/B, with a special interest in MED/Q’s genomic signatures that may contribute to the highly invasive nature of this emerging insect pest.ResultsThe genomes of both species share similarity in syntenic blocks, but have significant divergence in the gene coding sequence. Expansion of cytochrome P450 monooxygenases and UDP glycosyltransferases in MED/Q and MEAM1/B genome is functionally validated for mediating insecticide resistance in MED/Q using in vivo RNAi. The amino acid biosynthesis pathways in MED/Q genome are partitioned among the host and endosymbiont genomes in a manner distinct from other hemipterans. Evidence of horizontal gene transfer to the host genome may explain their obligate relationship. Putative loss-of-function in the immune deficiency-signaling pathway due to the gene loss is a shared ancestral trait among hemipteran insects.ConclusionsThe expansion of detoxification genes families, such as P450s, may contribute to the development of insecticide resistance traits and a broad host range in MED/Q and MEAM1/B, and facilitate species’ invasions into intensively managed cropping systems. Numerical and compositional changes in multiple gene families (gene loss and gene gain) in the MED/Q genome sets a foundation for future hypothesis testing that will advance our understanding of adaptation, viral transmission, symbiosis, and plant-insect-pathogen tritrophic interactions.

Altered hemoglobin co-factor sensitivity does not underlie the evolution of derived fossorial specializations in the family Talpidae.

The high O2 affinity of European mole (Talpa europaea) blood is postulated to largely arise from the presence of two β-globin chain residues (β4 Ser and β5 Gly) that weaken the interaction of its hemoglobin (Hb) with the red cell organophosphate 2,3-diphosphoglycerate (DPG). This latter trait is generally accepted to be an 'adaptation to subterranean life', despite the fact that no data are available for more basal mole lineages that have no evolutionary history of fossoriality (i.e. the ambulatory, high-elevation shrew-like moles and the semi-aquatic desmans), and which may similarly benefit from an elevated blood O2 affinity. To test whether evolution of a low DPG sensitivity phenotype is linked to derived fossorial lifestyles or represents an ancestral trait for the family, we determined the globin gene sequences and measured the intrinsic O2 affinity and co-factor sensitivity of the major Hb component of the gracile shrew-like mole (Uropsilus gracilis) and the Pyrenean desman (Galemys pyrenaicus). Our results unequivocally demonstrate that the presence of β4 Ser and β5 Gly, together with a low DPG sensitivity Hb phenotype, predates the radiation of the family Talpidae, and hence did not evolve as a specific adaptation to fossorial life. By contrast, our comparative analyses suggest that variations in whole blood O2 affinity among members of this family predominantly arose from amino acid substitutions that increase or decrease the intrinsic O2 affinity of the protein.

Modular patterns in behavioural evolution: webs derived from orbs

AbstractImperfect knowledge of ancestral behaviour often hampers tracing behavioural evolution. This limitation is reduced in orb weaving spiders, because spider orb web construction behaviour and the cues used by modern orb-weavers are well-studied and highly conserved. Several species in orb-weaving families build non-orb webs that are clearly derived from orbs, allowing transitions from ancestral to modern behaviours to be described with high confidence. Three major patterns of general evolutionary significance were found in 69 phylogenetically independent transitions in 15 groups in 8 families: ancestral traits were often maintained as units; the most frequent of the eight different types of ancestral trait change was transfer of an ancestral behaviour to a new context; and ‘new’ traits that had no clear homology with ancestral traits were also common. Changes occurred in all major stages of orb construction. This may be the most extensive summary of evolutionary transitions in behaviour yet compiled.

A Notch-regulated proliferative stem cell zone in the developing spinal cord is an ancestral vertebrate trait.

Vertebrates have evolved the most sophisticated nervous systems we know. These differ from the nervous systems of invertebrates in several ways, including the evolution of new cell types, and the emergence and elaboration of patterning mechanisms to organise cells in time and space. Vertebrates also generally have many more cells in their central nervous systems than invertebrates, and an increase in neural cell number may have contributed to the sophisticated anatomy of the brain and spinal cord. Here, we study how increased cell number evolved in the vertebrate central nervous system, investigating the regulation of cell proliferation in the lamprey spinal cord. Markers of proliferation show that a ventricular progenitor zone is found throughout the lamprey spinal cord. We show that inhibition of Notch signalling disrupts the maintenance of this zone. When Notch is blocked, progenitor cells differentiate precociously, the proliferative ventricular zone is lost and differentiation markers become expressed throughout the spinal cord. Comparison with other chordates suggests that the emergence of a persistent Notch-regulated proliferative progenitor zone was a crucial step for the evolution of vertebrate spinal cord complexity.