Ancient fig wasps indicate at least 34 Myr of stasis in their mutualism with fig trees

Fig wasps and fig trees are mutually dependent, with each of the 800 or so species of fig trees (Ficus, Moraceae) typically pollinated by a single species of fig wasp (Hymenoptera: Agaonidae). Molecular evidence suggests that the relationship existed over 65 Ma, during the Cretaceous. Here, we record the discovery of the oldest known fossil fig wasps, from England, dated at 34 Ma. They possess pollen pockets that contain fossil Ficus pollen. The length of their ovipositors indicates that their host trees had a dioecious breeding system. Confocal microscopy and scanning electron microscopy reveal that the fossil female fig wasps, and more recent species from Miocene Dominican amber, display the same suite of anatomical characters associated with fig entry and pollen-carrying as modern species. The pollen is also typical of modern Ficus. No innovations in the relationship are discernible for the last tens of millions of years.     

First reliable record of a fossil species of Anthomyiidae (Diptera), with comments on the definition of recent and fossil clades in phylogenetic classification

All previous records of fossil Anthomyiidae are shown to be unsubstantiated. A female anthomyiid of a new genus and species is hereby described from a piece of Dominican amber (Upper Eocene-Oligocene). Character analysis suggests that the fossil, Coenosopsites poinari gen. & sp. nov. , belongs to a Neotropical clade with two recent genera, Phaonantho Albuquerque and Coenosopsia Malloch. Evidence for a sister-group relationship between Coenosopsites poinari and the genus Coenosopsia is provided. Clades are the only acceptable units of phylogenetic classification. Combining fossil and recent clades in phylogenetic classification requires them to be temporally delimited. Proper application of phylogenetic definitions is essential for this purpose. It is proposed that the units of phylogenetic classification should be taxa for recent clades and plesia for fossil clades. A taxon is defined as node-based with reference to its recent species, while a plesion is defined as apomorphy-based. The term lineage is proposed for a recent clade defined as stem-based with reference to its recent sister group. Individual recent species represent clades that can be incorporated into phylogenetic classification as minimal taxon units. Individual fossil species may not represent clades and thus do not count as proper units of phylogenetic classification. However, the names of fossil species are readily construed also to signify plesia with the fossil species as their only known component. As such, they are proper units of phylogenetic classification.     

Introduced delicacy or native species? A natural origin of Bermudian terrapins supported by fossil and genetic data

Humans have greatly altered the natural distribution of species, making it difficult to distinguish between natural and introduced populations. This is a problem for conservation efforts because native or introduced status can determine whether a species is afforded protection or persecuted as an invasive pest. Holocene colonization events are especially difficult to discern, particularly when the species in question is a naturally good disperser and widely transported by people. In this study, we test the origin of such a species, the diamondback terrapin (Malaclemys terrapin), on Bermuda using a combination of palaeontologic (fossil, radiometric and palaeoenvironmental) and genetic data. These lines of evidence support the hypothesis that terrapins are relatively recent (between 3000 and 400 years ago) natural colonizers of Bermuda. The tiny population of Bermudian terrapins represents the second naturally occurring non-marine reptile that still survives on one of the most densely populated and heavily developed oceanic islands in the world. We recommend that they should be given protection as a native species.     

Miocene honey bees from the Randeck Maar of southwestern Germany (Hymenoptera, Apidae)

The Miocene Randeck Maar (southwestern Germany) is one of the only sites with abundant material of fossil honey bees. The fauna has been the focus of much scrutiny by early authors who recognized multiple species or subspecies within the fauna. The history of work on the Randeck Maar is briefly reviewed and these fossils placed into context with other Tertiary and living species of the genus Apis Linnaeus (Apinae: Apini). Previously unrecorded specimens from Randeck Maar were compared with earlier series in an attempt to evaluate the observed variation. A morphometric analysis of forewing venation angles across representative Recent and Tertiary species of Apis as well as various non-Apini controls was undertaken to evaluate the distribution of variation in fossil honey bees. The resulting dendrogram shows considerable variation concerning the wing venation of Miocene Apini, but intergradation of other morphological characters reveals no clear pattern of separate species. This suggests that a single, highly variable species was present in Europe during the Miocene. The pattern also supports the notion that the multiple species and subspecies proposed by earlier authors for the Randeck Maar honey bee fauna are not valid, and all are accordingly recognized as Apis armbrusteri Zeuner.     

A gharial from the Oligocene of Puerto Rico: transoceanic dispersal in the history of a non-marine reptile

The Indian gharial (Gavialis gangeticus) is not found in saltwater, but the geographical distribution of fossil relatives suggests a derivation from ancestors that lived in, or were at least able to withstand, saline conditions. Here, we describe a new Oligocene gharial, Aktiogavialis puertoricensis, from deltaic-coastal deposits of northern Puerto Rico. It is related to a clade of Neogene gharials otherwise restricted to South America. Its geological and geographical settings, along with its phylogenetic relationships, are consistent with two scenarios: (i) that a single trans-Atlantic dispersal event during the Tertiary explains the South American Neogene gharial assemblage and (ii) that stem gharials were coastal animals and their current restriction to freshwater settings is a comparatively recent environmental shift for the group. This discovery highlights the importance of including fossil information in a phylogenetic context when assessing the ecological history of modern organisms.     

Evolution of seahorses' upright posture was linked to Oligocene expansion of seagrass habitats

Seahorses (Syngnathidae: Hippocampus) are iconic marine teleosts that are readily identifiable by their upright posture. The fossil record is inadequate to shed light on the evolution of this trait because it lacks transitional forms. There are, however, extant syngnathid species (the pygmy pipehorses) that look like horizontally swimming seahorses and that might represent a surviving evolutionary link between the benthic seahorses and other, free-swimming members of the family Syngnathidae. Using sequence data from five nuclear loci, we confirm the sister taxon relationship between seahorses and pygmy pipehorses. Molecular dating indicates that the two taxa diverged during the Late Oligocene. During this time, tectonic events in the Indo-West Pacific resulted in the formation of vast amounts of new shallow-water areas and associated expansion of seagrass habitats that would have favoured the seahorses’ upright posture by improving their camouflage while not affecting their manoeuvrability negatively. The molecular techniques employed here provide new insights into the evolution of a taxon whose fossil record is incomplete, but whose evolutionary history is so recent that the major stages of morphological evolution are still represented in extant species.     

Taxonomic revision and phylogenetic analysis of the flightless Mancallinae (Aves, Pan-Alcidae)

Although flightless alcids from the Miocene and Pliocene of the eastern Pacific Ocean have been known for over 100 years, there is no detailed evaluation of diversity and systematic placement of these taxa. This is the first combined analysis of morphological and molecular data to include all extant alcids, the recently extinct Great Auk Pinguinus impennis, the mancalline auks, and a large outgroup sampling of 29 additional non-alcid charadriiforms. Based on the systematic placement of Mancallinae outside of crown clade Alcidae, the clade name Pan-Alcidae is proposed to include all known alcids. An extensive review of the Mancallinae fossil record resulted in taxonomic revision of the clade, and identification of three new species. In addition to positing the first hypothesis of inter-relationships between Mancallinae species, phylogenetic results support placement of Mancallinae as the sister taxon to all other Alcidae, indicating that flightlessness evolved at least twice in the alcid lineage. Convergent osteological characteristics of Mancallinae, the flightless Great Auk, and Spheniscidae are summarized, and implications of Mancallinae diversity, radiation, and extinction in the context of paleoclimatic changes are discussed.     

On the placement of the Cretaceous orthopteran Brauckmannia groeningae from Brazil, with notes on the relationships of Schizodactylidae (Orthoptera, Ensifera)

The fossil orthopteran Brauckmannia groeningae Martins-Neto (Orthoptera, Ensifera) from the Early Cretaceous Crato Formation of Brazil, currently misplaced at both the genus and family level, is transferred to the family Schizodactylidae and assigned to the extant genus Schizodactylus Brullé; ergo, Brauckmannia enters synonymy under Schizodactylus and Brauckmanniidae enters synonymy under Schizodactylidae. Schizodactylus groeningae (Martins-Neto), comb. n. agrees in size and general habitus with extant members of the genus, but can be readily separated by the robust, subovoid form of the metatibiae and the distinctive morphology of the lateral metabasitarsal processes. This species represents the first fossil occurrence of Schizodactylidae and the only New World record of this ancient lineage. Phylogenetic relationships of the schizodactylids are reviewed and a sister-group relationship with Grylloidea advocated based on a reappraisal of morphological and molecular evidence.     

The earliest fossil record of Panorpidae (Mecoptera) from the Middle Jurassic of China

The early history of Panorpidae (Mecoptera) is poorly known due to sparse fossil records. Up to date, only nine fossil species have been described, all from the Paleogene, except the Early Cretaceous Solusipanorpa gibbidorsa Lin, 1980. However, we suggest S. gibbidorsa is too incompletely preserved to permit even family classification. A new genus with two new species, Jurassipanorpa impunctata gen. et sp. n. and Jurassipanorpa sticta sp. n., are described based on four well-preserved specimens from the late Middle Jurassic Jiulongshan Formation of Daohugou, Inner Mongolia, China. These two new species are the earliest fossil records of Panorpidae. The new genus is erected based on a combination of forewing characters: both R₁ and Rs₁ with two branches, 1A reaching posterior margin of wing distad of the forking of Rs from R_1, and no crossveins or only one crossvein between veins of 1A and 2A. In all four specimens, long and robust setae ranging from 0.09 to 0.38 mm in length and pointing anteriorly, are present on anal veins of forewings. The function of these setae is enigmatic.     

A fossil brain from the Cretaceous of European Russia and avian sensory evolution

Fossils preserving traces of soft anatomy are rare in the fossil record; even rarer is evidence bearing on the size and shape of sense organs that provide us with insights into mode of life. Here, we describe unique fossil preservation of an avian brain from the Volgograd region of European Russia. The brain of this Melovatka bird is similar in shape and morphology to those of known fossil ornithurines (the lineage that includes living birds), such as the marine diving birds Hesperornis and Enaliornis, but documents a new stage in avian sensory evolution: acute nocturnal vision coupled with well-developed hearing and smell, developed by the Late Cretaceous (ca 90Myr ago). This fossil also provides insights into previous 'bird-like' brain reconstructions for the most basal avian Archaeopteryx--reduction of olfactory lobes (sense of smell) and enlargement of the hindbrain (cerebellum) occurred subsequent to Archaeopteryx in avian evolution, closer to the ornithurine lineage that comprises living birds. The Melovatka bird also suggests that brain enlargement in early avians was not correlated with the evolution of powered flight.     

Phylogeny of the cycads based on multiple single-copy nuclear genes: congruence of concatenated parsimony,likelihood and species tree inference methods

Background and aims

Despite a recent new classification, a stable phylogeny for the cycads has been elusive, particularly regarding resolution of Bowenia, Stangeria and Dioon. In this study, five single-copy nuclear genes (SCNGs) are applied to the phylogeny of the order Cycadales. The specific aim is to evaluate several gene tree–species tree reconciliation approaches for developing an accurate phylogeny of the order, to contrast them with concatenated parsimony analysis and to resolve the erstwhile problematic phylogenetic position of these three genera.

Methods

DNA sequences of five SCNGs were obtained for 20 cycad species representing all ten genera of Cycadales. These were analysed with parsimony, maximum likelihood (ML) and three Bayesian methods of gene tree–species tree reconciliation, using Cycas as the outgroup. A calibrated date estimation was developed with Bayesian methods, and biogeographic analysis was also conducted.

Key Results

Concatenated parsimony, ML and three species tree inference methods resolve exactly the same tree topology with high support at most nodes. Dioon and Bowenia are the first and second branches of Cycadales after Cycas, respectively, followed by an encephalartoid clade (Macrozamia–Lepidozamia–Encephalartos), which is sister to a zamioid clade, of which Ceratozamia is the first branch, and in which Stangeria is sister to Microcycas and Zamia.

Conclusions

A single, well-supported phylogenetic hypothesis of the generic relationships of the Cycadales is presented. However, massive extinction events inferred from the fossil record that eliminated broader ancestral distributions within Zamiaceae compromise accurate optimization of ancestral biogeographical areas for that hypothesis. While major lineages of Cycadales are ancient, crown ages of all modern genera are no older than 12 million years, supporting a recent hypothesis of mostly Miocene radiations. This phylogeny can contribute to an accurate infrafamilial classification of Zamiaceae.     

Comparative application of the coefficient of variation and range-based statistics for assessing the taxonomic composition of fossil samples

Dental variation has been used commonly to assess taxonomic composition in morphologically homogeneous fossil samples. While the coefficient of variation (CV) has been used traditionally, range-based measures of variation, such as the range as a percentage of the mean (R%) and the maximum/minimum index (I_max/min) have recently become popular alternatives. The current study compares the performance of these statistics when applied to single- and pooled-species dental samples of extant Cercopithecus species. A common methodology for such problems of species discrimination has been to simply compare the maximum value of a variation statistic observed in extant samples with that observed in the fossil sample. However, regardless of what statistic is used, this approach has an unknowable Type I error rate, and usually has low power to detect multiple species. A more appropriate method involves a formal hypothesis test. The null hypothesis is that the level of variation in the fossil sample does not exceed what might be expected in a sample drawn randomly from a reference population, taking into account sampling error and the size of the fossil sample. Previous research using this method with the CV has indicated that it offers considerable power at an acceptable Type I error rate. In the current study, the data of primary interest were posterior dental dimensions for single- and pooled species samples from extant Cercopithecus species. In addition, the study also investigated the relative performance of variation statistics when applied to highly dimorphic canine dimensions, since much recent work has employed sexually dimorphic dental dimensions for assessing single-species hypotheses. The results indicate that the CV consistently out-performed the range-based statistics when using posterior dental dimensions to test a single-species hypothesis. Regardless of which statistic was used, tests on sexually dimorphic dimensions offered minimal power. In consideration of these results and the problem of studywise Type I error rates, we recommend against the use of multiple measures of variation to test for multiple species composition, and advocate the CV as the statistic of choice when using the method of Cope & Lacy (1992). For similar reasons, we argue for careful selection of dental variables for inclusion in such analyses, and in particular recommend against including sexually dimorphic dimensions when testing for multiple species composition.     

Mites of the genus Neharpyrhynchus Fain (Acariformes, Harpirhynchidae) from Neotropical birds

Three new species of parasitic mites of the genus Neharpyrhynchus Fain (Acariformes, Harpirhynchidae) are described from Neotropical birds: Neharpyrhynchus chlorospingussp. n. from Chlorospingus pileatus (Passeriformes, Emberizidae) from Costa Rica, Neharpyrhynchus mironovisp. n. from Dacnys cayana (Passeriformes, Thraupidae) and Neharpyrhynchus tangarasp. n. from Tangara cayana (Thraupidae) both from Brazil. Neharpyrhynchus trochilinus (Fain) is recorded from 3 new host species of the family Trochilidae (Apodiformes), Panterpe insignis and Eugenes fulgens from Costa Rica, and Amazilia lactea from Brazil. Emended diagnosis of the genus and a key to species are provided; all records of Neharpyrhynchus species are summarized.     

Variation in enamel thickness within the genus Homo

Recent humans and their fossil relatives are classified as having thick molar enamel, one of very few dental traits that distinguish hominins from living African apes. However, little is known about enamel thickness in the earliest members of the genus Homo, and recent studies of later Homo report considerable intra- and inter-specific variation. In order to assess taxonomic, geographic, and temporal trends in enamel thickness, we applied micro-computed tomographic imaging to 150 fossil Homo teeth spanning two million years. Early Homo postcanine teeth from Africa and Asia show highly variable average and relative enamel thickness (AET and RET) values. Three molars from South Africa exceed Homo AET and RET ranges, resembling the hyper thick Paranthropus condition. Most later Homo groups (archaic European and north African Homo, and fossil and recent Homo sapiens) possess absolutely and relatively thick enamel across the entire dentition. In contrast, Neanderthals show relatively thin enamel in their incisors, canines, premolars, and molars, although incisor AET values are similar to H. sapiens. Comparisons of recent and fossil H. sapiens reveal that dental size reduction has led to a disproportionate decrease in coronal dentine compared with enamel (although both are reduced), leading to relatively thicker enamel in recent humans. General characterizations of hominins as having ‘thick enamel’ thus oversimplify a surprisingly variable craniodental trait with limited taxonomic utility within a genus. Moreover, estimates of dental attrition rates employed in paleodemographic reconstruction may be biased when this variation is not considered. Additional research is necessary to reconstruct hominin dietary ecology since thick enamel is not a prerequisite for hard-object feeding, and it is present in most later Homo species despite advances in technology and food processing.     

Caught in the act: the first record of copulating fossil vertebrates

The behaviour of fossil organisms can typically be inferred only indirectly, but rare fossil finds can provide surprising insights. Here, we report from the Eocene Messel Pit Fossil Site between Darmstadt and Frankfurt, Germany numerous pairs of the fossil carettochelyid turtle Allaeochelys crassesculpta that represent for the first time among fossil vertebrates couples that perished during copulation. Females of this taxon can be distinguished from males by their relatively shorter tails and development of plastral kinesis. The preservation of mating pairs has important taphonomic implications for the Messel Pit Fossil Site, as it is unlikely that the turtles would mate in poisonous surface waters. Instead, the turtles initiated copulation in habitable surface waters, but perished when their skin absorbed poisons while sinking into toxic layers. The mating pairs from Messel are therefore more consistent with a stratified, volcanic maar lake with inhabitable surface waters and a deadly abyss.     

Evolution of unusual morphologies in Lentibulariaceae (bladderworts and allies) and Podostemaceae (river-weeds): a pictorial report at the interface of developmental biology and morphological diversification

Background Various groups of flowering plants reveal profound (‘saltational’) changes of their bauplans (architectural rules) as compared with related taxa. These plants are known as morphological misfits that appear as rather large morphological deviations from the norm. Some of them emerged as morphological key innovations (perhaps ‘hopeful monsters’) that gave rise to new evolutionary lines of organisms, based on (major) genetic changes.Scope This pictorial report places emphasis on released bauplans as typical for bladderworts (Utricularia, approx. 230 secies, Lentibulariaceae) and river-weeds (Podostemaceae, three subfamilies, approx. 54 genera, approx. 310 species). Bladderworts (Utricularia) are carnivorous, possessing sucking traps. They live as submerged aquatics (except for their flowers), as humid terrestrials or as epiphytes. Most Podostemaceae are restricted to rocks in tropical river-rapids and waterfalls. They survive as submerged haptophytes in these extreme habitats during the rainy season, emerging with their flowers afterwards. The recent scientific progress in developmental biology and evolutionary history of both Lentibulariaceae and Podostemaceae is summarized.Conclusions Lentibulariaceae and Podostemaceae follow structural rules that are different from but related to those of more typical flowering plants. The roots, stems and leaves – as still distinguishable in related flowering plants – are blurred (‘fuzzy’). However, both families have stable floral bauplans. The developmental switches to unusual vegetative morphologies facilitated rather than prevented the evolution of species diversity in both families. The lack of one-to-one correspondence between structural categories and gene expression may have arisen from the re-use of existing genetic resources in novel contexts. Understanding what developmental patterns are followed in Lentibulariaceae and Podostemaceae is a necessary prerequisite to discover the genetic alterations that led to the evolution of these atypical plants. Future molecular genetic work on morphological misfits such as bladderworts and river-weeds will provide insight into developmental and evolutionary aspects of more typical vascular plants.     

A new proposal concerning the botanical origin of Baltic amber

Baltic amber constitutes the largest known deposit of fossil plant resin and the richest repository of fossil insects of any age. Despite a remarkable legacy of archaeological, geochemical and palaeobiological investigation, the botanical origin of this exceptional resource remains controversial. Here, we use taxonomically explicit applications of solid-state Fourier-transform infrared (FTIR) microspectroscopy, coupled with multivariate clustering and palaeobotanical observations, to propose that conifers of the family Sciadopityaceae, closely allied to the sole extant representative, Sciadopitys verticillata, were involved in the genesis of Baltic amber. The fidelity of FTIR-based chemotaxonomic inferences is upheld by modern–fossil comparisons of resins from additional conifer families and genera (Cupressaceae: Metasequoia; Pinaceae: Pinus and Pseudolarix). Our conclusions challenge hypotheses advocating members of either of the families Araucariaceae or Pinaceae as the primary amber-producing trees and correlate favourably with the progressive demise of subtropical forest biomes from northern Europe as palaeotemperatures cooled following the Eocene climate optimum.     

New fossil records of Tapirus (Mammalia, Perissodactyla) from Brazil, with a critical analysis of intra-generic diversity assessments based on lower molar size variability

A large set of South American fossils belonging to the genus Tapirus has been described on the basis of differences in size and proportions of lower molariform teeth. Nevertheless, the reliability of dental proportions for the diagnosis of fossil tapir species is controversial. In this paper, we describe new fossil material of Tapirus from the Quaternary of Serra da Bodoquena, Southwestern Brazil, comparing it to other fossil and extant specimens of the genus by means of multivariate morphometric analyses of lower molariform teeth linear dimensions. The results of Principal Component Analyses indicate that some of the extant and extinct material attributed to Tapirus fall within the range of variation in size and proportions of lower molariform teeth exhibited by recent species of the genus. Therefore, part of the fossil material attributed to new species or to Tapirus sp. may be referable to the extant species Tapirus terrestris. We conclude that the sole use of lower molariform teeth size and proportions to erect new species of Tapirus may not be reliable, and therefore we advocate caution when describing fossil tapirs exclusively based on these criteria.     

An analysis of two Myosorex species (Soricidae) from the Early Pliocene site of Langebaanweg (West coast, South Africa) using geometric morphometrics, linear measurements, and non-metric characters

This represents the first study of the soricid community from the Early Pliocene site of Langebaanweg (LBW) which is represented by four species, two of which belong to the soricid genus Myosorex (Forest shrew). Using geometric morphometrics the two Myosorex fossil species are compared with each other, and the extant western and eastern Cape species: Myosorex varius, M. cafer and M. longicaudatus. In addition, the results from an analysis of a number of non-metric characters and linear measurements on the fossil species are presented. The mandibles of the fossil species are characterized by extremely broad teeth, ascending rami which are relatively gracile and differ in shape and size from modern species, and the existence of a number of primitive features of the mandibles and teeth. This evidence is interpreted as indicating that the two LBW Myosorex species represent an archaic lineage now extinct in southern Africa.