A phylogenetic comparative method for evaluating trait coevolution across two phylogenies for sets of interacting species

Evaluating trait correlations across species within a lineage via phylogenetic regression is fundamental to comparative evolutionary biology, but when traits of interest are derived from two sets of lineages that coevolve with one another, methods for evaluating such patterns in a dual‐phylogenetic context remain underdeveloped. Here, we extend multivariate permutation‐based phylogenetic regression to evaluate trait correlations in two sets of interacting species while accounting for their respective phylogenies. This extension is appropriate for both univariate and multivariate response data, and may use one or more independent variables, including environmental covariates. Imperfect correspondence between species in the interacting lineages can also be accommodated, such as when species in one lineage associate with multiple species in the other, or when there are unmatched taxa in one or both lineages. For both univariate and multivariate data, the method displays appropriate type I error, and statistical power increases with the strength of the trait covariation and the number of species in the phylogeny. These properties are retained even when there is not a 1:1 correspondence between lineages. Finally, we demonstrate the approach by evaluating the evolutionary correlation between traits in fig species and traits in their agaonid wasp pollinators. R computer code is provided.     

Evolutionary history of lamprey paired species Lampetra fluviatilis (L.) and Lampetra planeri (Bloch) as inferred from mitochondrial DNA variation

A remarkable trend in the evolution of lampreys is the occurrence in most genera of 'paired species', in which the parasitic anadromous lampreys are believed to have given rise to nonparasitic freshwater resident populations. The present work examines the phylogeography of the European paired species Lampetra fluviatilis and Lampetra planeri, in an attempt to elucidate species pair evolutionary history. We studied sequence variation in cytochrome b and ATPase 6, 8 mitochondrial genes in 63 individuals from 21 localities of the paired species throughout their distribution range. Results from the phylogenetic and nested clade analyses were largely consistent, suggesting the existence of three major evolutionary lineages: lineage I and possibly lineage II are widespread throughout Europe, while the most ancestral lineage III is apparently restricted to the Iberian Peninsula. The high genetic diversity observed in the Iberian Peninsula is probably the result of refugial persistence and subsequent accumulation of variation over several ice ages, whereas the low levels of genetic diversity observed in central and northern Europe should reflect a rapid postglacial colonization. Results suggest that L. planeri originated within at least two distinct evolutionary lineages, rejecting the single origin hypothesis. The observed lack of taxa monophyly within lineage I may be the result of ongoing gene flow if the two taxa are alternate life-history forms of a single species. However, structure within lineage I is also consistent with the hypothesis of divergence of taxa after postglacial dispersion (around 2000 generations ago) with incomplete lineage sorting. Further testing of the alternative hypotheses is warranted.     

Cryptic speciation in the field vole: a multilocus approach confirms three highly divergent lineages in Eurasia

Species are generally described from morphological features, but there is growing recognition of sister forms that show substantial genetic differentiation without obvious morphological variation and may therefore be considered ‘cryptic species’. Here, we investigate the field vole (Microtus agrestis), a Eurasian mammal with little apparent morphological differentiation but which, on the basis of previous sex‐linked nuclear and mitochondrial DNA (mtDNA) analyses, is subdivided into a Northern and a Southern lineage, sufficiently divergent that they may represent two cryptic species. These earlier studies also provided limited evidence for two major mtDNA lineages within Iberia. In our present study, we extend these findings through a multilocus approach. We sampled 163 individuals from 46 localities, mainly in Iberia, and sequenced seven loci, maternally, paternally and biparentally inherited. Our results show that the mtDNA lineage identified in Portugal is indeed a distinct third lineage on the basis of other markers as well. In fact, multilocus coalescent‐based methods clearly support three separate evolutionary units that may represent cryptic species: Northern, Southern and Portuguese. Divergence among these units was inferred to have occurred during the last glacial period; the Portuguese lineage split occurred first (estimated at c. 70 000 bp ), and the Northern and Southern lineages separated at around the last glacial maximum (estimated at c. 18 500 bp ). Such recent formation of evolutionary units that might be considered species has repercussions in terms of understanding evolutionary processes and the diversity of small mammals in a European context.     

Global phylogeographic limits of Hawaii's avian malaria

The introduction of avian malaria (Plasmodium relictum) to Hawaii has provided a model system for studying the influence of exotic disease on naive host populations. Little is known, however, about the origin or the genetic variation of Hawaii's malaria and traditional classification methods have confounded attempts to place the parasite within a global ecological and evolutionary context. Using fragments of the parasite mitochondrial gene cytochrome b and the nuclear gene dihydrofolate reductase-thymidylate synthase obtained from a global survey of greater than 13000 avian samples, we show that Hawaii's avian malaria, which can cause high mortality and is a major limiting factor for many species of native passerines, represents just one of the numerous lineages composing the morphological parasite species. The single parasite lineage detected in Hawaii exhibits a broad host distribution worldwide and is dominant on several other remote oceanic islands, including Bermuda and Moorea, French Polynesia. The rarity of this lineage in the continental New World and the restriction of closely related lineages to the Old World suggest limitations to the transmission of reproductively isolated parasite groups within the morphological species.     

A (not-so-radical) solution to the species problem

What are species? One popular answer is that species are individuals. Here I develop another approach to thinking about species, an approach based on the notion of a lineage. A lineage is a sequence of reproducing entities, individuated in terms of its components. I argue that one can conceive of species as groups of lineages, either organism lineages or population lineages. Conceiving of species as groups of lineages resolves the problems that the individual conception of species is supposed to resolve. It has added the virtue of focusing attention on the characteristic of species that is most relevant to understanding their role in evolutionary processes, namely, the lineage structure of species.     

Repeated evolution of queen parthenogenesis and social hybridogenesis in Cataglyphis desert ants

Over the last decade, genetic studies on social insects have revealed a remarkable diversity of unusual reproductive strategies, such as male clonality, female clonality, and social hybridogenesis. In this context, Cataglyphis desert ants are useful models because of their unique reproductive systems. In several species, queens conditionally use sexual reproduction and parthenogenesis to produce sterile workers and reproductive queens, respectively. In social hybridogenesis, two distinct genetic lineages coexist within a population, and workers result from mating between partners of different lineages; in contrast, queens and males are both produced asexually by parthenogenesis. Consequently, nonreproductive workers are all interlineage hybrids, whereas reproductives are all pure lineage individuals. Here, we characterized the reproductive systems of 11 species to investigate the distribution of the conditional use of sex and social hybridogenesis in Cataglyphis. We identified one new case in which sexual reproduction was conditionally used in the absence of dependent‐lineage reproduction. We also discovered five new instances of social hybridogenesis. Based on our phylogenetic analyses, we inferred that both the conditional use of sex and social hybridogenesis independently evolved multiple times in the genus Cataglyphis.     

Bio-cultural effects in medieval populations

Male skeletons from medieval archaeological sites are analysed to assess differences in stature and body proportions related to the bio-cultural environment, such as social, economic, and health factors. Environmental factors, such as climate change in the course of the Middle Ages, did not have statistically significant effect on body proportions in these samples. The results show a relationship between bio-cultural factors and physique in the analysed populations that indicate stunted growth in height and weight in a leprosarium population with a low socio-economic and health status. A high-status monastic population is characterised by a stocky build, i.e., increased weight for height and relatively shorter limbs, while a medieval parish population has a linear build, i.e., relatively long limbs for height and decreased weight for height. These characteristics, relative weight for height and relative limb length, changed during the course of the Middle Ages, as did stature.     

Evolving lineages of Symbiodinium-like dinoflagellates based on ITS1 rDNA

Symbiodinium-like dinoflagellates have been shown to be a diverse group of endosymbionts that associate mutualistically with many kinds of coral reef dwellers, including cnidarians, molluscs, and protists. A high number of genetically ITS types of symbionts have been reported to date. However, whether these recently identified Symbiodinium ITS types indeed represent independent evolutionary lineages is still unsettled. Here I tested the null hypothesis that certain group of symbionts sampled from different geographical locations are derived from a single evolutionary lineage using a nested clade analysis (NCA). I analyzed a total of 174 ITS1 sequences from GenBank and pooled them into 74 ITS1 distinct haplotypes. Using these haplotypes, the statistical parsimony criterion produced 23 independent network trees, each one corresponding to a genetically independent evolving lineage. Some of these lineages revealed certain degree of specificity with some host groups at least at the phylum level. Within the previously described 28S-rDNA phylotype A, five ITS1 lineages were resolved. Phylotypes B and C resolved each in two ITS1 lineages. The highest ITS1 symbiont diversity was observed within the phylotype F, in which 11 lineages were resolved. Moreover, most of these lineages were associated uniquely with protist hosts from the group of foraminiferans. Here it is suggested that this high genetic diversity of endosymbionts associated with foraminiferans is linked with the evolution of soritacean foraminifera, which seems to have been driven by endosymbiosis. Lastly, the absence of genetic recombination presented in this study, suggest a lack of hybridisation at least among the major 28S-rDNA phylotypes within Symbiodinium-like dinoflagellates. This supports highly the idea that these phylotypes are indeed independent evolutionary units, which should be considered at least as different species. Whether they belong to the same genus or to different higher taxa still needs to be revised.     

Comparative phylogeography of pitvipers suggests a consensus of ancient Middle American highland biogeography

Aim  We used inferences of phylogenetic relationships and divergence times for three lineages of highland pitvipers to identify broad-scale historical events that have shaped the evolutionary history of Middle American highland taxa, and to test previous hypotheses of Neotropical speciation.
Location  Middle America (Central America and Mexico).
Methods  We used 2306 base pairs of mitochondrial gene sequences from 178 individuals to estimate the phylogeny and divergence times of New World pitviper lineages, focusing on three genera ( Atropoides , Bothriechis and Cerrophidion ) that are broadly co-distributed across Middle American highlands.
Results  We found strong correspondence across three highland lineages for temporally and geographically coincident divergences in the Miocene and Pliocene, and further identified widespread within-species divergences across multiple lineages that occurred in the early–middle Pleistocene.
Main conclusions  Available data suggest that there were at least three major historical events in Middle America that had broad impacts on species divergence and lineage diversification among highland taxa. In addition, we find widespread within-species genetic structure that may be attributable to the climatic changes that affected gene flow among highland taxa during the middle–late Pleistocene.     

Out of the Pan-Himalaya: Evolutionary history of the Paeoniaceae revealed by phylogenomics

Peonies (the Paeoniaceae, Paeonia L.) are famous garden flowers, medicinal plants, and edible oil crops, but their evolutionary history largely remains unknown. To probe into their phylogenetic relationships, evolutionary history, formation of present distribution pattern, and origins of tetraploids, we sequenced 25 fragments belonging to 20 single copy nuclear genes and 14 chloroplast regions of all species in the genus to reconstruct phylogenetic relationships, date the divergence times of lineages, infer the ancestral biogeographical regions, and document the parents of tetraploids. Our results show that Paeoniaceae separated from the other members in Saxifragales in the Campanian of the late Cretaceous and diverged into two clades, woody and herbaceous clades, in the late Oligocene or early Miocene. They survived and early diverged in the Pan-Himalaya where they migrated eastwards to East Asia and further to NW America, and northwards to Middle Asia, and further to Europe. The woody lineage differentiated into two sublineages with accelerated root or floral disk evolution, while the herbaceous lineage diverged into five sublineages. Multiple glacial and interglacial cycles in Europe in the late Pliocene and early Pleistocene created opportunities for the peony species to meet and hybridize in the Mediterranean refugia, giving rise to eight allotetraploid species and four infraspecific tetraploids. Paeonia daurica Andrews, P. obovata Maxim., and P. tenuifolia L. served as the most important parents. The phylogeny of Paeonia L. implies that a new taxonomic system with two subgenera and seven sections should be proposed.     

Cryptic biodiversity and phylogeographical patterns in a snapping shrimp species complex

Recent investigations suggest that marine biodiversity may be much higher than earlier estimates, and an important hidden source of diversity in marine systems is the phenomenon of cryptic species complexes. Such complexes are informative models for research into the evolutionary processes that govern species compositions of marine fauna. The snapping shrimp genera Alpheus and Synalpheus are known to harbour large numbers of cryptic species; here, I characterize the genetic structure of the Alpheus armillatus species complex in the northern Caribbean, west Atlantic, and Gulf of Mexico using mitochondrial and nuclear sequence data. Over this geographical region, the complex harbours at least three lineages that are probable reproductively isolated species; all major lineages diverged subsequent to the close of the Isthmus of Panama. Only one lineage was present in the Gulf of Mexico, whereas outside the Gulf of Mexico there was no clear tendency for lineage dominance by geographical region, as most sites were populated by shrimp from at least two lineages. However, within each lineage, there was strong evidence of population genetic differentiation between geographical regions. All lineages showed strong signals of demographic expansion, and one lineage showed sharply reduced genetic diversity, suggestive of past population bottlenecks or recently founded populations with low gene flow from other sites. These results show that evolutionary processes leading to divergence and speciation have been common and recent in the snapping shrimp, and suggest that connectivity among shrimp populations may be limited.     

Early to high medieval colonization and alluvial landscape transformation of the Labe valley (Czech Republic): evaluation of archaeological,pollen and macrofossil evidence

In the High Middle Ages, a wave of landscape transformation which originated in western Europe swept across the east-central part of the subcontinent. In the Czech Republic, this happened during the 13th century and it had the same environmental attributes as in the rest of Europe—a considerable increase in population, vast deforestation resulting in a rapid increase in soil erosion, irreversible changes in forest species composition and overall formation of a cultural landscape. In the Czech Republic, the dynamics of such a radical change are poorly understood because it would require detailed archaeological, historical and palaeoecological insight into developments during the Early Middle Ages—a demand that is mostly not met. The aim of this paper is to fill in this gap. Archaeological and historical data from three early medieval strongholds located in central Bohemia, at Libice nad Cidlinou, Stará Boleslav and Hradi??ko, are summarized and evaluated. The first two sites represent well-known political and religious centres of the early Czech state in the 10 to 11th centuries, while the last was of secondary importance. These archaeological sites have radiocarbon dated pollen and plant macrofossil evidence from oxbow sedimentary sequences which are situated in the immediate vicinity of the strongholds. The issue of fluvial transport of pollen and macrofossils is also discussed. Both pollen and macrofossil data from Hradi??ko show surprisingly small impact of the stronghold on the forested alluvial environment. The vicinity of Stará Boleslav was intensively affected by human activity only during the later 11th century. It has not been possible to trace any impact of the foundation of the stronghold at Libice nad Cidlinou on the landscape. Medieval landscape change began before the 13th century in some places, as shown by the data from Stará Boleslav.     

Mitochondrial DNA phylogeography of the three-spined stickleback (Gasterosteus aculeatus) in Europe-evidence for multiple glacial refugia

An analysis of mitochondrial DNA sequence variation in 172 three-spined sticklebacks (Gasterosteus aculeatus) sampled across the European distribution range revealed three major evolutionary lineages occupying relatively large and separate geographic areas. The trans-Atlantic lineage comprised of populations spanning from the East Coast of USA to the continental Europe and was basal group to the other European lineages in the phylogeny. The European lineage included populations located in the Western and Eastern Europe, British Isles, Scandinavia as well as some parts of the Mediterranean region. The third lineage was specific to the Black Sea drainages. The within lineage structure was characterized by significant excess of low frequency haplotypes and star-like mtDNA genealogies, which suggest a recent population expansions to the formerly glaciated marine and freshwater environments. A coalescent-based method dated the splits between the major lineages to have occurred during the Saalian and Weichselian glaciations in the late Pleistocene, depending on the molecular clock calibration. The coalescent simulations further indicate high degree of genetic diversity within the lineages and a substantial increase in the genetic diversity in the European lineage relative to the ancestral level. In addition to the three major lineages, the freshwater populations in R. Neretva and L. Skadar in the Adriatic Sea coast region harboured unique and highly divergent haplotypes suggesting long independent histories of these populations. Evidence from mtDNA analyses suggests that these populations deserve a status of an evolutionary significant unit.     

Paleolithic and neolithic lineages in the European mitochondrial gene pool.

Phylogenetic and diversity analysis of the mtDNA control region sequence variation of 821 individuals from Europe and the Middle East distinguishes five major lineage groups with different internal diversities and divergence times. Consideration of the diversities and geographic distribution of these groups within Europe and the Middle East leads to the conclusion that ancestors of the great majority of modern, extant lineages entered Europe during the Upper Paleolithic. A further set of lineages arrived from the Middle East much later, and their age and geographic distribution within Europe correlates well with archaeological evidence for two culturally and geographically distinct Neolithic colonization events that are associated with the spread of agriculture. It follows from this interpretation that the major extant lineages throughout Europe predate the Neolithic expansion and that the spread of agriculture was a substantially indigenous development accompanied by only a relatively minor component of contemporary Middle Eastern agriculturalists. There is no evidence of any surviving Neanderthal lineages among modern Europeans.     

ITS-1 ribosomal DNA sequence variants are maintained in different species and strains of Echinococcus

This study investigated sequence heterogeneity in the first internal transcribed spacer (ITS-1) of ribosomal DNA within and among species and strains of Echinococcus. Different ITS-1 sequence variants exist in Echinococcus granulosus and Echinococcus multilocularis, which represent at least four evolutionary lineages: (1) a sheep strain-lineage of E. granulosus, (2) a sister lineage of a cervid and camel E. granulosus ITS-1 variants, (3) a lineage including the ITS-1 variants representing horse, bovine and camel strains of E. granulosus, as well as variants from E. multilocularis, Echinococcus oligarthrus and Echinococcus vogeli and (4) a distinct lineage of ITS-1 variants including E. granulosus strains from sheep and cervid, and E. multilocularis. At least two of the species (E. granulosus and E. multilocularis) were paraphyletic for ITS-1. Divergent ITS-1 variants from these two species shared distinct evolutionary lineages. The sequence data provided evidence that at least two turnover mechanisms, namely slippage and unequal crossing over/transposition, have led to the divergence and maintenance of sequence variants in Echinococcus species and strains.     

Valkyries: Was gender equality high in the Scandinavian periphery since Viking times? Evidence from enamel hypoplasia and height ratios

Scandinavian countries currently have very high values of female autonomy. Was this already the case in Viking Times? In this study, we trace the roots of gender equality in the Scandinavian periphery over the past two millennia. We evaluate and recommend a new measure of early gender equality: relative enamel hypoplasia values of males and females. This new indicator allows us to trace relative health and nutritional equality, using archaeological evidence. We find that Scandinavian women in the rural periphery already had relatively good health and nutritional values during the Viking era and the medieval period thereafter. The corresponding value is 0.8 equality advantage for Scandinavian women, whereas in the rest of Europe most values fall in a band around 1.2 ratio units. This suggests that the currently high gender equality had a precedence during the Middle Ages.     

The ups and downs of the building trade in a medieval city: Tree-ring data as proxies for economic,social and demographic dynamics in Bruges (c. 1200–1500)

The exceptional preservation of the cityscape in the medieval city of Bruges (Belgium) triggered dendrochronological research on numerous preserved roof constructions in historical buildings, that date from the Middle Ages up to the early modern period. As many of these oak timbers lack the preservation of waney edge, a method was developed to combine sapwood estimates of felling dates within each building phase and to compute a summed probability distribution (SPD) for those felling dates. These summed probabilities now allow us to reconstruct temporal trends in building trade activity in an expanding medieval city. When linked to the social status of the patrons of the building projects, it is observed that resilience to demographic crisis and political turmoil differs among the social groups and political elite of a medieval society. Furthermore the dating results of decades of tree-ring research now provide a typo-chronological framework of roof constructions and shows that it took nearly two centuries before more advanced technological skill in the construction of roofs completely replaced the traditional common rafter roofs.     

CRANIAL SIZE VARIATION AND LINEAGE DIVERSITY IN EARLY PLEISTOCENE HOMO

A recent article in this journal concluded that a sample of early Pleistocene hominin crania assigned to genus Homo exhibits a pattern of size variation that is time dependent, with specimens from different time periods being more different from each other, on average, than are specimens from the same time period. The authors of this study argued that such a pattern is not consistent with the presence of multiple lineages within the sample, but rather supports the hypothesis that the fossils represent an anagenetically evolving lineage (i.e., an evolutionary species). However, the multiple‐lineage models considered in that study do not reflect the multiple‐species alternatives that have been proposed for early Pleistocene Homo. Using simulated data sets, I show that fossil assemblages that contain multiple lineages can exhibit the time‐dependent pattern of variation specified for the single‐lineage model under certain conditions, particularly when temporal overlap among fossil specimens attributed to the lineages is limited. These results do not reject the single‐lineage hypothesis, but they do indicate that rejection of multiple lineages in the early Pleistocene Homo fossil record is premature, and that other sources of variation, such as differences in cranial shape, should be considered.     

Using regional comparative phylogeographic data from snake lineages to infer historical processes in Middle America

Understanding how historical processes have either similarly, or differentially, shaped the evolution of lineages or biotic assemblages is important for a broad spectrum of fields. Gaining such understanding can be particularly challenging, however, especially for regions that have a complex geologic and biological history. In this study we apply a broad comparative approach to distill such regional biogeographic perspectives, by characterizing sets of divergence times for major biogeographic boundaries estimated from multiple codistributed lineages of snakes. We use a large combined (mitochondrial gene sequence) phylogeographic/phylogenetic dataset containing several clades of snakes that range across Middle America – the tropical region between Mexico and northwestern South America. This region is known for its complex tectonic history, and poorly understood historical biogeography. Based on our results, we highlight how phylogeographic transition zones between Middle and South America and the Nicaragua Depression appear to have undergone multiple episodes of diversification in different lineages. This is in contrast to other examples we find where apparently a single vicariant period is shared across multiple lineages. We specifically evaluate the distributions of divergence time estimates across multiple lineages and estimate the number of temporal periods of lineage diversification per biogeographic break. Overall, our results highlight a great deal of shared temporal divergence, and provide important hypotheses for yet unstudied lineages. These multi‐lineage comparisons across multiple spatial and temporal scales provide excellent predictive power for identifying the roles of geology, climate, ecology and natural history in shaping regional biodiversity.     

Biogeography of Triassic tetrapods: evidence for provincialism and driven sympatric cladogenesis in the early evolution of modern tetrapod lineages

Triassic tetrapods are of key importance in understanding their evolutionary history, because several tetrapod clades, including most of their modern lineages, first appeared or experienced their initial evolutionary radiation during this Period. In order to test previous palaeobiogeographical hypotheses of Triassic tetrapod faunas, tree reconciliation analyses (TRA) were performed with the aim of recovering biogeographical patterns based on phylogenetic signals provided by a composite tree of Middle and Late Triassic tetrapods. The TRA found significant evidence for the presence of different palaeobiogeographical patterns during the analysed time spans. First, a Pangaean distribution is observed during the Middle Triassic, in which several cosmopolitan tetrapod groups are found. During the early Late Triassic a strongly palaeolatitudinally influenced pattern is recovered, with some tetrapod lineages restricted to palaeolatitudinal belts. During the latest Triassic, Gondwanan territories were more closely related to each other than to Laurasian ones, with a distinct tetrapod fauna at low palaeolatitudes. Finally, more than 75 per cent of the cladogenetic events recorded in the tetrapod phylogeny occurred as sympatric splits or within-area vicariance, indicating that evolutionary processes at the regional level were the main drivers in the radiation of Middle and Late Triassic tetrapods and the early evolution of several modern tetrapod lineages.