Prolonged faunal turnover in earliest ants revealed by North American Cretaceous amber.

All ∼14,000 extant ant species descended from the same common ancestor, which lived ∼140-120 million years ago (Ma).1,2 While modern ants began to diversify in the Cretaceous, recent fossil evidence has demonstrated that older lineages concomitantly occupied the same ancient ecosystems.3 These early-diverging ant lineages, or stem ants, left no modern descendants; however, they dominated the fossil record throughout the Cretaceous until their ultimate extinction sometime around the K-Pg boundary. Even as stem ant lineages appear to be diverse and abundant throughout the Cretaceous, the extent of their longevity in the fossil record and circumstances contributing to their extinction remain unknown.3 Here we report the youngest stem ants, preserved in ∼77 Ma Cretaceous amber from North Carolina, which illustrate unexpected morphological stability and lineage persistence in this enigmatic group, rivaling the longevity of contemporary ants. Through phylogenetic reconstruction and morphometric analyses, we find evidence that total taxic turnover in ants was not accompanied by a fundamental morphological shift, in contrast to other analogous stem extinctions such as theropod dinosaurs. While stem taxa showed broad morphological variation, high-density ant morphospace remained relatively constant through the last 100 million years, detailing a parallel, but temporally staggered, evolutionary history of modern and stem ants.

Trait-Based Paleontological Niche Prediction Recovers Extinct Ecological Breadth of the Earliest Specialized Ant Predators.

AbstractPaleoecological estimation is fundamental to the reconstruction of evolutionary and environmental histories. The ant fossil record preserves a range of species in three-dimensional fidelity and chronicles faunal turnover across the Cretaceous and Cenozoic; taxonomically rich and ecologically diverse, ants are an exemplar system to test new methods of paleoecological estimation in evaluating hypotheses. We apply a broad extant ecomorphological dataset to evaluate random forest machine learning classification in predicting the total ecological breadth of extinct and enigmatic hell ants. In contrast to previous hypotheses of extinction-prone arboreality, we find that hell ants were primarily leaf litter or ground-nesting and foraging predators, and by comparing ecospace occupations of hell ants and their extant analogs, we recover a signature of ecomorphological turnover across temporally and phylogenetically distinct lineages on opposing sides of the Cretaceous-Paleogene boundary. This paleoecological predictive framework is applicable across lineages and may provide new avenues for testing hypotheses over deep time.

Community form, function and phylogenetic diversity respond differently across microhabitat and recovery gradients.

Research Highlight: Hoenle, P. O., Staab, M., Donoso, D. A., Argoti, A., & Blüthgen, N. (2023). Stratification and recovery time jointly shape ant functional reassembly in a neotropical forest. Journal of Animal Ecology, https://doi.org/10.1111/1365-2656.13896. Space, time and abiotic variation are primary axes across investigations of community ecology and disturbed ecosystems offer tractable systems for assessing their relative impact. While recovering forests can act as isolated case studies in understanding community assembly, it is not well understood how individual microhabitats respond to recovery and ultimately shape community attributes. Hoenle et al. (2023) leverage the ubiquity and microhabitat-specific diversity of ants across a gradient from active agricultural sites to old-growth forest and assess how recovery and stratification together shape communities. The authors find distinct stratification across phylogenetic, functional and trait diversity as forest recovery time increases, while also recovering unique recovery trajectories contingent on trait sampling. While stratified, phylogenetic and functional diversity did not increase along this recovery gradient. Ten out of 13 sampled traits were jointly influenced by both stratification and recovery time. In contrast to intuitive predictions, a majority of trait means converged throughout the recovery period. Results highlight the multifaceted nature of recovery-based community assembly and the capacity of multidimensional sampling to uncover surprising patterns in ecologically diverse lineages.

Deep time extinction of largest insular ant predators and the first fossil Neoponera (Formicidae: Ponerinae) from Miocene age Dominican amber.

BACKGROUND: Ponerine ants are almost exclusively predatory and comprise many of the largest known ant species. Within this clade, the genus Neoponera is among the most conspicuous Neotropical predators. We describe the first fossil member of this lineage: a worker preserved in Miocene-age Dominican amber from Hispaniola. RESULTS: Neoponera vejestoria sp. nov. demonstrates a clear case of local extinction-there are no known extant Neoponera species in the Greater Antilles. The species is attributable to an extant and well-defined species group in the genus, which suggests the group is older than previously estimated. Through CT scan reconstruction and linear morphometrics, we reconstruct the morphospace of extant and fossil ants to evaluate the history and evolution of predatory taxa in this island system. CONCLUSIONS: The fossil attests to a shift in insular ecological community structure since the Miocene. The largest predatory taxa have undergone extinction on the island, but their extant relatives persist throughout the Neotropics. Neoponera vejestoria sp. nov. is larger than all other predatory ant workers known from Hispaniola, extant or extinct. Our results empirically demonstrate the loss of a functional niche associated with body size, which is a trait long hypothesized to be related to extinction risk.

Evaluation of Fossil Amber Birefringence and Inclusions Using Terahertz Time-Domain Spectroscopy.

Using a cross-polarization transmission geometry, stress maps for the normalized birefringence and intrinsic stress direction of polymeric materials may be obtained using terahertz nondestructive evaluation. The analysis method utilizes a deconvolution method to determine the arrival times and amplitude of the cross-polarized terahertz pulses through a birefringent material. Using amber (a naturally occurring polymer) as a material of interest, stress maps show that inclusion-free Lebanese amber samples behave as classic uniaxial birefringent (photoelastic) materials whose principal stress directions, as inferred in the terahertz spectral range, agree well with visible photoelasticity measurements. Since amber samples, depending upon their source, may be either transparent or opaque to visible light, comparing birefringence measurements in the visible and terahertz spectral ranges cross-validates the stress measurements, thereby establishing a strong and unique stress analysis methodology for visibly opaque samples. While the material of interest for this paper is amber, the method is generally applicable for any terahertz-transparent polymer. The cross-polarization experimental configuration enables stress levels within the amber matrix to be visualized while also outlining highly localized regions of stress surrounding inclusions. Birefringence stress maps clearly show localized increases in stress magnitude and directional changes surrounding inclusions.

An Eocene army ant.

Among social insects, army ants are exceptional in their voracious coordinated predation, nomadic life history and highly specialized wingless queens: the synthesis of these remarkable traits is referred to as the army ant syndrome. Despite molecular evidence that the army ant syndrome evolved twice during the mid-Cenozoic, once in the Neotropics and once in the Afrotropics, fossil army ants are markedly scarce, comprising a single known species from the Caribbean 16 Ma. Here we report the oldest army ant fossil and the first from the Eastern Hemisphere (EH), Dissimulodorylus perseus, preserved in Baltic amber dated to the Eocene. Using a combined morphological and molecular ultra conserved elements dataset spanning doryline lineages, we find that D. perseus is nested among extant EH army ants with affinities to Dorylus. Army ants are characterized by limited extant diversification throughout most of the Cenozoic; the discovery of D. perseus suggests an unexpected diversity of now-extinct army ant lineages in the Cenozoic, some of which were present in Continental Europe.

Non-destructive comparative evaluation of fossil amber using terahertz time-domain spectroscopy.

Fossilized plant resins, or ambers, offer a unique paleontological window into the history of life. A natural polymer, amber can preserve aspects of ancient environments, including whole organisms, for tens or even hundreds of millions of years. While most amber research involves imaging with visual light, other spectra are increasingly used to characterize both organismal inclusions as well as amber matrix. Terahertz (THz) radiation, which occupies the electromagnetic band between microwave and infrared light wavelengths, is non-ionizing and frequently used in polymer spectroscopy. Here, we evaluate the utility of amber terahertz spectroscopy in a comparative setting for the first time by analyzing the terahertz optical properties of samples from 10 fossil deposits ranging in age from the Miocene to the Early Cretaceous. We recover no clear relationships between amber age or botanical source and terahertz permittivity; however, we do find apparent deposit-specific permittivity among transparent amber samples. By comparing the suitability of multiple permittivity models across sample data we find that models with a distribution of dielectric relaxation times best describe the spectral permittivity of amber. We also demonstrate a process for imaging amber inclusions using terahertz transmission and find that terahertz spectroscopy can be used to identify some synthetic amber forgeries.

A tardigrade in Dominican amber.

Tardigrades are a diverse group of charismatic microscopic invertebrates that are best known for their ability to survive extreme conditions. Despite their long evolutionary history and global distribution in both aquatic and terrestrial environments, the tardigrade fossil record is exceedingly sparse. Molecular clocks estimate that tardigrades diverged from other panarthropod lineages before the Cambrian, but only two definitive crown-group representatives have been described to date, both from Cretaceous fossil deposits in North America. Here, we report a third fossil tardigrade from Miocene age Dominican amber. Paradoryphoribius chronocaribbeus gen. et sp. nov. is the first unambiguous fossil representative of the diverse superfamily Isohypsibioidea, as well as the first tardigrade fossil described from the Cenozoic. We propose that the patchy tardigrade fossil record can be explained by the preferential preservation of these microinvertebrates as amber inclusions, coupled with the scarcity of fossiliferous amber deposits before the Cretaceous.

Comparative mitochondrial genomics of sponge-dwelling snapping shrimps in the genus Synalpheus: Exploring differences between eusocial and non-eusocial species and insights into phylogenetic relationships in caridean shrimps.

The genus Synalpheus is a cosmopolitan clade of marine shrimps found in most tropical regions. Species in this genus exhibit a range of social organizations, including pair-forming, communal breeding, and eusociality, the latter only known to have evolved within this genus in the marine realm. This study examines the complete mitochondrial genomes of seven species of Synalpheus and explores differences between eusocial and non-eusocial species considering that eusociality has been shown before to affect the strength of purifying selection in mitochondrial protein coding genes. The AT-rich mitochondrial genomes of Synalpheus range from 15,421 bp to 15,782 bp in length and comprise, invariably, 13 protein-coding genes (PCGs), two ribosomal RNA genes, and 22 transfer RNA genes. A 648 bp to 994 bp long intergenic space is assumed to be the D-loop. Mitochondrial gene synteny is identical among the studied shrimps. No major differences occur between eusocial and non-eusocial species in nucleotide composition and codon usage profiles of PCGs and in the secondary structure of tRNA genes. Maximum likelihood phylogenetic analysis of the complete concatenated PCG complement of 90 species supports the monophyly of the genus Synalpheus and its family Alpheidae. Moreover, the monophyletic status of the caridean families Alvinocaridae, Atyidae, Thoridae, Lysmatidae, Palaemonidae, and Pandalidae within caridean shrimps are fully or highly supported by the analysis. We therefore conclude that mitochondrial genomes contain sufficient phylogenetic information to resolve relationships at high taxonomic levels within the Caridea. Our analysis of mitochondrial genomes in the genus Synalpheus contributes to the understanding of the coevolution between genomic architecture and sociality in caridean shrimps and other marine organisms.

Eusociality Shapes Convergent Patterns of Molecular Evolution across Mitochondrial Genomes of Snapping Shrimps.

Eusociality is a highly conspicuous and ecologically impactful behavioral syndrome that has evolved independently across multiple animal lineages. So far, comparative genomic analyses of advanced sociality have been mostly limited to insects. Here, we study the only clade of animals known to exhibit eusociality in the marine realm-lineages of socially diverse snapping shrimps in the genus Synalpheus. To investigate the molecular impact of sociality, we assembled the mitochondrial genomes of eight Synalpheus species that represent three independent origins of eusociality and analyzed patterns of molecular evolution in protein-coding genes. Synonymous substitution rates are lower and potential signals of relaxed purifying selection are higher in eusocial relative to noneusocial taxa. Our results suggest that mitochondrial genome evolution was shaped by eusociality-linked traits-extended generation times and reduced effective population sizes that are hallmarks of advanced animal societies. This is the first direct evidence of eusociality impacting genome evolution in marine taxa. Our results also strongly support the idea that eusociality can shape genome evolution through profound changes in life history and demography.

Specialized Predation Drives Aberrant Morphological Integration and Diversity in the Earliest Ants.

Extinct haidomyrmecine "hell ants" are among the earliest ants known [1, 2]. These eusocial Cretaceous taxa diverged from extant lineages prior to the most recent common ancestor of all living ants [3] and possessed bizarre scythe-like mouthparts along with a striking array of horn-like cephalic projections [4-6]. Despite the morphological breadth of the fifteen thousand known extant ant species, phenotypic syndromes found in the Cretaceous are without parallel and the evolutionary drivers of extinct diversity are unknown. Here, we provide a mechanistic explanation for aberrant hell ant morphology through phylogenetic reconstruction and comparative methods, as well as a newly reported specimen. We report a remarkable instance of fossilized predation that provides direct evidence for the function of dorsoventrally expanded mandibles and elaborate horns. Our findings confirm the hypothesis that hell ants captured other arthropods between mandible and horn in a manner that could only be achieved by articulating their mouthparts in an axial plane perpendicular to that of modern ants. We demonstrate that the head capsule and mandibles of haidomyrmecines are uniquely integrated as a consequence of this predatory mode and covary across species while finding no evidence of such modular integration in extant ant groups. We suggest that hell ant cephalic integration-analogous to the vertebrate skull-triggered a pathway for an ancient adaptive radiation and expansion into morphospace unoccupied by any living taxon.

The complete mitochondrial genome of the eusocial sponge-dwelling snapping shrimp Synalpheus microneptunus.

In the marine realm, eusociality is only known to have evolved within a clade of sponge-dwelling snapping shrimps in the genus Synalpheus. Deciphering the genomic underpinnings of eusociality in these marine shrimps has been limited by the sparse genomic resources in this genus. Here, we report, for a eusocial shrimp Synalpheus microneptunus, a complete mitochondrial genome (22X coverage) assembled from short Illumina 150 bp paired-end reads. The 15,603 bp long mitochondrial genome of S. microneptunus is AT-rich and includes 13 protein-coding genes (PCGs), 2 ribosomal RNA genes, 22 transfer RNA genes and an 834 bp intergenic region assumed to be the D-loop. The gene order is identical to that reported for most caridean shrimps and corresponds to the presumed Pancrustacean ground pattern. All PCGs showed signs of purifying selection, with KA/KS <<1 across the whole PCGs and most sliding windows within PCGs. Maximum-likelihood and Bayesian inference phylogenetic analyses of 13 PCGs and 68 terminals supports the monophyly of the Caridea and the family Alpheidae. The complete mitochondrial genome of the eusocial shrimp Synalpheus microneptunus will contribute to a better understanding of the selective pressures and rates of molecular evolution in marine eusocial animals.

Fossil amber reveals springtails' longstanding dispersal by social insects.

BACKGROUND: Dispersal is essential for terrestrial organisms living in disjunct habitats and constitutes a significant challenge for the evolution of wingless taxa. Springtails (Collembola), the sister-group of all insects (with Diplura), are reported since the Lower Devonian and are thought to have originally been subterranean. The order Symphypleona is reported since the early Cretaceous with genera distributed on every continent. This distribution implies an ability to disperse over oceans, however symphypleonan Collembola have never been reported in marine water contrary to other springtail orders. Despite being highly widespread, modern springtails are rarely reported in any kind of biotic association. Interestingly, the fossil record has provided occasional occurrences of Symphypleona attached by the antennae onto the bodies of larger arthropods. RESULTS: Here, we document the case of a ~ 16 Ma old fossil association: a winged termite and ant displaying not some, but 25 springtails attached or in close proximity to the body. The collembola exhibit rare features for fossils, reflecting their courtship and phoretic behaviours. By observing the modes of attachment of springtails on different arthropods, the sex representation and ratios in springtail antennal anatomies in new and previously reported cases, we infer a likely mechanism for dispersal in Symphypleona. By revealing hidden evidence of modern springtail associations with other invertebrates such as ants and termites, new compelling assemblages of fossil springtails, and the drastic increase of eusocial insects' abundance during the Cenozoic (ants/termites comprising more than a third of insects in Miocene amber), we stress that attachment on winged castes of ants and termites may have been a mechanism for the worldwide dispersal of this significant springtail lineage. Moreover, by comparing the general constraints applying to the other wingless soil-dwelling arthropods known to disperse through phoresy, we suggest biases in the collection and observation of phoretic Symphypleona related to their reflexive detachment and infer that this behaviour continues today. CONCLUSIONS: The specific case of tree resin entrapment represents the (so far) only condition uncovering the phoretic dispersal mechanism of springtails - one of the oldest terrestrial arthropod lineages living today.

Giant ants and their shape: revealing relationships in the genus Titanomyrma with geometric morphometrics.

Shape is a natural phenomenon inherent to many different lifeforms. A modern technique to analyse shape is geometric morphometrics (GM), which offers a whole range of methods concerning the pure shape of an object. The results from these methods have provided new insights into biological problems and have become especially useful in the fields of entomology and palaeontology. Despite the conspicuous successes in other hymenopteran groups, GM analysis of wings and fossil wings of Formicidae has been neglected. Here we tested if landmarks defining the wing shape of fossil ants that belong to the genus Titanomyrma are reliable and if this technique is able to expose relationships among different groups of the largest Hymenoptera that ever lived. This study comprises 402 wings from 362 ants that were analysed and assigned with the GM methods linear discriminant function analysis, principal component analysis, canonical variate analysis, and regression. The giant ant genus Titanomyrma and the parataxon Formicium have different representatives that are all very similar but these modern methods were able to distinguish giant ant types even to the level of the sex. Thirty-five giant ant specimens from the Eckfeld Maar were significantly differentiable from a collection of Messel specimens that consisted of 187 Titanomyrma gigantea females and 42 T. gigantea males, and from 74 Titanomyrma simillima females and 21 T. simillima males. Out of the 324 Messel ants, 127 are newly assigned to a species and 223 giant ants are newly assigned to sex with GM analysis. All specimens from Messel fit to the two species. Moreover, shape affinities of these groups and the species Formicium brodiei, Formicium mirabile, and Formicium berryi, which are known only from wings, were investigated. T. gigantea stands out with a possible female relative in one of the Eckfeld specimens whereas the other groups show similar shape patterns that are possibly plesiomorphic. Formicidae are one of the most dominant taxa in the animal kingdom and new methods can aid in investigating their diversity in the present and in deep time. GM of the ant wing delivers significant results and this core of methods is able to enhance the toolset we have now to analyse the complex biology of the ants. It can prove as especially useful in the future when incorporated into better understanding aspects of evolutionary patterns and ant palaeontology.

Incorporating fossils into hypotheses of insect phylogeny.

Fossils represent stem and crown lineages, and their inclusion in phylogenetic reconstruction influences branch lengths, topology, and divergence time estimation. In addition, paleontological data may inform trends in morphological evolution as well as biogeographic history. Here we review the incorporation of fossils in studies of insect evolution, from morphological analyses to combined 'total evidence' node dating analyses. We discuss challenges associated with fossil based phylogenetics, and suggest best practices for use in tree reconstruction.

Adaptive Radiation in Socially Advanced Stem-Group Ants from the Cretaceous.

Across terrestrial ecosystems, modern ants are ubiquitous. As many as 94 out of every 100 individual arthropods in rainforests are ants, and they constitute up to 15% of animal biomass in the Amazon. Moreover, ants are pervasive agents of natural selection as over 10,000 arthropod species are specialized inquilines or myrmecomorphs living among ants or defending themselves through mimicry. Such impact is traditionally explained by sociality: ants are the first major group of ground-dwelling predatory insects to become eusocial, increasing efficiency of tasks and establishing competitive superiority over solitary species. A wealth of specimens from rich deposits of 99 million-year-old Burmese amber resolves ambiguity regarding sociality and diversity in the earliest ants. The stem-group genus Gerontoformica maintained distinct reproductive castes including morphotypes unknown in solitary aculeate (stinging) wasps, providing insight into early behavior. We present rare aggregations of workers, indicating group recruitment as well as an instance of interspecific combat; such aggression is a social feature of modern ants. Two species and an unusual new genus are described, further expanding the remarkable diversity of early ants. Stem-group ants are recovered as a paraphyletic assemblage at the base of modern lineages varying greatly in size, form, and mouthpart structure, interpreted here as an adaptive radiation. Though Cretaceous stem-group ants were eusocial and adaptively diverse, we hypothesize that their extinction resulted from the rise of competitively superior crown-group taxa that today form massive colonies, consistent with Wilson and Hölldobler's concept of "dynastic succession."

Morphologically Specialized Termite Castes and Advanced Sociality in the Early Cretaceous.

A hallmark of animals that are eusocial, or those with advanced sociality, is reproductive specialization into worker and queen castes. In the most derived societies, these divisions are essentially fixed and in some arthropods, include further specialization--a tripartite system with a soldier caste that defends the colony. Eusociality has originated numerous times among insects but is believed to have appeared first in the termites (Isoptera), in the Early Cretaceous. However, all termites known from the Cretaceous have, until now, only been winged reproductives (alates and dealates); the earliest soldiers and definitive workers were known from just the Miocene (ca. 17-20 million years ago [mya]). Here, we report six termite species preserved in Early Cretaceous (ca. 100 mya) amber from Myanmar, one described as Krishnatermes yoddha gen. et sp. nov., comprising the worker/pseudergate, winged reproductive, and soldier, and a second species, Gigantotermes rex gen. et sp. nov., based on one of the largest soldier termites yet known. Phylogenetic analysis indicates that Krishnatermes are in the basal "Meiatermes-grade" of Cretaceous termites. Workers/pseudergates of another four species are briefly described, but not named. One of these workers/pseudergates reveals that ants--the most serious enemies of modern termites--lived in close proximity to termites in the Burmese paleofauna. These discoveries demonstrate the Mesozoic antiquity of specialized termite caste systems and corroborate that among all social species, termites probably had the original societies.

A diverse ant fauna from the mid-cretaceous of Myanmar (Hymenoptera: Formicidae).

A new collection of 24 wingless ant specimens from mid-Cretaceous Burmese amber (Albian-Cenomanian, 99 Ma) comprises nine new species belonging to the genus Sphecomyrmodes Engel and Grimaldi. Described taxa vary considerably with regard to total size, head and body proportion, cuticular sculpturing, and petiole structure while all species are unified by a distinct shared character. The assemblage represents the largest known diversification of closely related Cretaceous ants with respect to species number. These stem-group ants exhibit some characteristics previously known only from their extant counterparts along with presumed plesiomorphic morphology. Consequently, their morphology may inform hypotheses relating to basal relationships and general patterns of ant evolution. These and other uncovered Cretaceous species indicate that stem-group ants are not simply wasp-like, transitional formicids, but rather a group of considerable adaptive diversity, exhibiting innovations analogous to what crown-group ants would echo 100 million years later.