Biology subjects

Linksvayer, T. A.

Publications and source records attributed to Linksvayer, T. A..

13 recordsLinked to original sources

bioRxiv2025

High-throughput phenomics of global ant biodiversity

The big data era in biology is underway, but the study of organismal form has been slow to capitalize on advances in imaging and computation. Modern imaging can digitize whole organisms, but low throughput has limited the effort to document morphological diversity. Within the open science initiative Antscan, we applied high-throughput synchrotron X-ray microtomography to capture phenotypes across a diverse and ecologically dominant insect group -- ants. We provide 2193 whole-body 3D ant datasets from 792 species to broadly cover the ant phylogeny with a global scope, also pairing phenomic data with genome sequencing projects. Scans acquired with standardized parameters facilitate automated analysis and free access to data can broaden the audience and incentivize methods development. Antscan presents a scalable approach to create libraries of diverse anatomies, heralding a new era of studies on the evolution, structure, and function of organismal phenotypes.

zoology↗

bioRxiv2025

Eusociality evolved at a much higher rate in haplodiploid insects

As a corollary to inclusive fitness theory, W.D. Hamiltons haplodiploid hypothesis proposed that eusociality evolves more readily in haplodiploids because of inflated genetic relatedness between sisters1. For the past sixty years, theoreticians have developed models clarifying how haplodiploidy might favor the evolution of eusociality2-5. Despite this sustained theoretical interest, the predicted relationship between haplodiploidy and eusociality has only very recently been empirically tested6,7. Here, we use two large species-level insect phylogenies with comprehensive sociality and ploidy trait data to test if eusociality evolves more readily in haplodiploids. We find that estimated transition rates to eusociality are higher in haplodiploids, but that this pattern is driven by a much higher transition rate within a single haplodiploid lineage, the aculeate Hymenoptera. Thus, the apparent links between haplodiploidy and eusociality reflect clade-specific dynamics rather than a general effect of haplodiploidy.

evolutionary biology↗

bioRxiv2024

Emergent Collective Behavior Evolves More Rapidly Than Individual Behavior Among Ant Species

Emergence is a fundamental concept in biology and other disciplines, but whether emergent phenotypes evolve similarly to non-emergent phenotypes is unclear. The hypothesized process of emergent evolution posits that evolutionary change in collective behavior is irreducible to evolutionary change in the intrinsic behaviors of isolated individuals. As a result, collective behavior might evolve more rapidly and diversify more between populations compared to individual behavior. To test if collective behavior evolves emergently, we conducted a large comparative study using 22 ant species and gathered over 1,500 behavioral rhythm time series from hundreds of colonies and isolated individuals, totaling over 1.5 years of behavioral data. We show that analogous traits measured at individual and collective levels exhibit distinct evolutionary patterns. The estimated rates of phenotypic evolution for the rhythmicity of activity in ant colonies were faster than the evolutionary rates of the same behavior measured in isolated individual ants, and total variation across species in collective behavior was higher than variation in individual behavior. We hypothesize that more rapid evolution and higher variation is a general feature of emergent phenotypes relative to lower-level phenotypes across complex biological systems.

evolutionary biology↗

bioRxiv2021

Genome-wide, genic, and site-specific changes associated with the convergent evolution of sociality in spiders

The transition from solitary to social life is a major phenotypic innovation, but its genetic underpinnings are largely unknown. To identify genomic changes associated with this transition, we compare the genomes of 22 spider species representing eight recent and independent origins of sociality. Hundreds of genes tend to experience shifts in selection during the repeated transition to social life. These genes are associated with several key functions, such as neurogenesis, behavior, and metabolism, and include genes that previously have been implicated in animal social behavior and human behavioral disorders. In addition, social species have elevated genome-wide rates of molecular evolution associated with relaxed selection caused by reduced effective population size. Altogether, our study provides unprecedented insights into the genomic signatures of social evolution and the specific genetic changes that repeatedly underpin the evolution of sociality. Our study also highlights the heretofore unappreciated potential of transcriptomics using ethanol-preserved specimens for comparative genomics and phylotranscriptomics.

evolutionary biology↗

bioRxiv2020

The collective behavior of ant groups depends on group genotypic composition

Increasingly, researchers document variation between groups in collective behavior, but the genetic architecture of collective behavior and how the genotypic composition of groups affects collective behavior remains unclear. Social insects are ideal for studying the effects of genetic variation on collective behavior because their societies are defined by social interactions. To explore how the genetic composition of groups affects collective behavior, we constructed groups of pharaoh ants (Monomorium pharaonis) from 33 genetically distinct colonies of known pedigree. The groups consisted of either all workers from the same single colony or workers from two genetically different colonies, and we assayed the exploration and aggression of the groups. We found that collective behavior depended on the specific genotypic combination of group members, i.e. we found evidence for genotype-by-genotype epistasis for both collective behaviors. Furthermore, the observed collective behavior of groups differed from the additive genetic expectations of groups, further demonstrating the importance of genotype-by-genotype effects. Finally, the collective aggression of the groups was negatively correlated with the pairwise relatedness estimates between workers within the group. Overall, this study highlights that specific combinations of genotypes influence group-level phenotypes and the difficulty of predicting group-level phenotypes using only additive models.

evolutionary biology↗

bioRxiv2019

Ant cuticular hydrocarbons are heritable and associated with variation in colony productivity

In social insects, cuticular hydrocarbons function in nestmate recognition and also provide a waxy barrier against desiccation, but basic evolutionary genetic features, including the heritability of hydrocarbon profiles and how they are shaped by natural selection are largely unknown. We used a new pharaoh ant (Monomorium pharaonis) laboratory mapping population to estimate the heritability of individual cuticular hydrocarbons, genetic correlations between hydrocarbons, and fitness consequences of phenotypic variation in the hydrocarbons. Individual hydrocarbons had low to moderate estimated heritability, indicating that some compounds provide more information about genetic relatedness and can also better respond to natural selection. Strong genetic correlations between compounds are likely to constrain independent evolutionary trajectories, which is expected given that many hydrocarbons share biosynthetic pathways. Variation in cuticular hydrocarbons was associated with variation in colony productivity, with some hydrocarbons experiencing strong directional selection. Altogether, our study builds on our knowledge of the genetic architecture of the social insect hydrocarbon profile and demonstrates that hydrocarbon variation is shaped by natural selection.

evolutionary biology↗

bioRxiv2019

Comparative genomics identifies putative signatures of sociality in spiders

Comparative genomics has begun to elucidate the genomic basis of social life in insects but insight into the genomic basis of spider sociality has lagged behind. To begin to characterize genomic signatures associated with the evolution of social life in spiders, we performed one of the first spider comparative genomics studies including five solitary species and two social species, representing two independent origins of sociality in the genus Stegodyphus. We found that the two social spider species had a large expansion of gene families associated with transport and metabolic processes and an elevated genome-wide rate of molecular evolution compared with the five solitary spider species. Genes that were rapidly evolving in the two social species relative to the five solitary species were enriched for transport, behavior, and immune functions, while genes that were rapidly evolving in the solitary species were enriched for energy metabolism processes. Most rapidly evolving genes in the social species S. dumicola were broadly expressed across four tissues and enriched for transport functions, but 12 rapidly evolving genes showed brain-specific expression and were enriched for social behavioral processes. Altogether, our study identifies putative genomic signatures and potential candidate genes associated with spider sociality. These results indicate that future spider comparative genomic studies, including broader sampling and additional independent origins of sociality, can further clarify the genomic causes and consequences of social life.

evolutionary biology↗

bioRxiv2019

The bacterial endosymbiont Wolbachia increases reproductive investment and accelerates the life cycle of ant colonies

Wolbachia is a widespread group of maternally-transmitted endosymbiotic bacteria that often manipulates the reproductive strategy and life history of its solitary hosts to enhance its own transmission. Wolbachia also commonly infects eusocial insects such as ants, although the effects of infection on social organisms remain largely unknown. We tested the effects of infection on colony-level reproduction and life history traits in the invasive pharaoh ant, Monomorium pharaonis. First we compared the reproductive investment of infected and uninfected colonies with queens of three discrete ages, and we found that infected colonies had increased reproductive investment. Next, we compared the long-term growth and reproduction of infected and uninfected colonies across their life cycle, and we found that infected colonies had increased colony-level growth and early colony reproduction. These colony-level effects of Wolbachia infection seem to result because of a live fast, die young life history strategy of infected queens. Such accelerated colony life cycle is likely beneficial for both the host and the symbiont and may have contributed to success of the highly invasive pharaoh ant.

evolutionary biology↗

bioRxiv2019

Ant collective behavior is heritable and shaped by selection

Collective behaviors are widespread in nature and usually assumed to be strongly shaped by natural selection. However, the degree to which variation in collective behavior is heritable and has fitness consequences -- the two prerequisites for evolution by natural selection -- is largely unknown. We used a new pharaoh ant (Monomorium pharaonis) mapping population to estimate the heritability, genetic correlations, and fitness consequences of three collective behaviors (foraging, aggression, and exploration) as well as body size, sex ratio, and caste ratio. Heritability estimates for the collective behaviors were moderate, ranging from 0.17 to 0.32, but lower than our estimates for the heritability of caste ratio, sex ratio, and the body size of new workers, queens, and males. Moreover, variation among colonies in collective behaviors was phenotypically correlated, suggesting that selection may shape multiple colony collective behaviors simultaneously. Finally, we found evidence for directional selection that was similar in strength to estimates of selection in natural populations. Altogether, our study begins to elucidate the genetic architecture of collective behavior and is one of the first studies to demonstrate that it is shaped by selection.

evolutionary biology↗

bioRxiv2019

Transcriptomic basis and evolution of the ant social interactome

Development is often strongly regulated by interactions among close relatives, but the underlying molecular mechanisms are largely unknown. In eusocial insects, interactions between caregiving worker nurses and larvae regulate larval development and resultant adult phenotypes. Here, we begin to characterize the social interactome regulating ant larval development by collecting and sequencing the transcriptomes of interacting nurses and larvae across time. We find that the majority of nurse and larval transcriptomes exhibit parallel expression dynamics across larval development. We leverage this widespread nurse-larva gene co-expression to infer putative social gene regulatory networks acting between nurses and larvae. Genes with the strongest inferred social effects tend to be peripheral elements of within-tissue regulatory networks and are often known to encode secreted proteins. This includes interesting candidates such as the nurse-expressed giant-lens, which may influence larval epidermal growth factor signaling, a pathway known to influence various aspects of insect development. Finally, we find that genes with the strongest signatures of social regulation tend to experience relaxed selective constraint and are evolutionarily young. Overall, our study provides a first glimpse into the molecular and evolutionary features of the social mechanisms that regulate all aspects of social life.\n\nAuthor SummarySocial interactions are fundamental to all forms of life, from single-celled bacteria to complex plants and animals. Despite their obvious importance, little is known about the molecular causes and consequences of social interactions. In this paper, we study the molecular basis of nurse-larva social interactions that regulate larval development in the pharaoh ant Monomorium pharaonis. We infer the effects of social interactions on gene expression from samples of nurses and larvae collected in the act of interaction across a developmental time series. Gene expression appears to be closely tied to these interactions, such that we can identify genes expressed in nurses with putative regulatory effects on larval gene expression. Genes which we infer to have strong social regulatory effects tend to have weak regulatory effects within individuals, and highly social genes tend to experience relatively weaker natural selection in comparison to less social genes. This study represents a novel approach and foundation upon which future studies at the intersection of genetics, behavior, and evolution can build.

evolutionary biology↗

bioRxiv2018

The convergent evolution of caste in ants and honey bees is based on a shared core of ancient reproductive genes and many plastic genes

Eusociality has convergently evolved multiple times, but the genomic basis of caste-based division of labor and degree to which independent origins of eusociality have utilized common genes remain largely unknown. Here we characterize caste-specific transcriptomic profiles across development and adult body segments from pharaoh ants (Monomorium pharaonis) and honey bees (Apis mellifera), representing two independent origins of eusociality. We identify a substantial shared core of genes upregulated in the abdomens of queen ants and honey bees that also tends to be upregulated in mated female flies, suggesting that these genes are part of a conserved insect reproductive groundplan. Outside of this shared groundplan, few genes are differentially expressed in common. Instead, the majority of the thousands of caste-associated genes are plastically-expressed, rapidly evolving, and relatively evolutionarily young. These results emphasize that the recruitment of both highly conserved and lineage-specific genes underlie the convergent evolution of novel traits such as eusociality.

evolutionary biology↗

bioRxiv2017

Ant nurse workers exhibit behavioral and transcriptomic specialization on larval stage but not caste

Division of labor within and between the worker and queen castes is thought to underlie the tremendous success of social insects. Colonies might benefit if subsets of nurse workers specialize further in caring for larvae of a certain stage or caste, given that larval nutritional requirements depend on stage and caste. We used short- (<1 hr) and long-term (ten days) behavioral observations to determine whether nurses of the pharaoh ant (Monomorium pharaonis) exhibit such specialization. We found that nurses were behaviorally specialized based on larval instar but not on larval caste. This specialization was widespread, with 56% of nurses in the short-term and between 22-27% in the long-term showing significant specialization. Additionally, we identified [~]200 genes that were differentially expressed in nurse head and abdominal tissues between nurses feeding young versus old larvae. These included 18 genes predicted to code for secreted proteins, which may be passed from nurses to larvae via trophallaxis, as well as vitellogenin and major royal jelly protein-1, which have previously been implicated in the transfer of nutrition from nurse to larvae and the regulation of larval development and caste in social insects. Altogether, our results provide the first evidence in any social insect for a division of labor among nurse workers based on larval stage, and our study begins to elucidate the molecular mechanisms underlying this specialization.

evolutionary biology↗

bioRxiv2017

Pharaoh ant colonies dynamically regulate colony demography by culling young queen and male-destined larvae

The success of social insect colonies is dependent upon efficient and dynamic allocation of resources to alternate queen and worker castes. The developmental and molecular mechanisms regulating the caste fate of individual larvae in response to environmental cues have been the focus of intense study. However, the mechanisms regulating colony-level resource allocation into alternate castes (i.e. caste allocation ratios) are less well studied. Here, we systematically manipulate colony demography to elucidate the social regulatory mechanisms of caste allocation in the ant Monomorium pharaonis. We find that differences in caste allocation result from differences in timing and efficiency of culling of very young reproductive-destined larvae, which are always present in colonies. Based on our results, we develop a conceptual model depicting how colonies integrate numerous individual-level caste determination decisions to regulate colony-level caste allocation. We propose that adult workers make decisions about culling larvae based on the ratio of the number of workers to the number of eggs contained in colonies, likely signalled by pheromone present on eggs. This strategy is a bet-hedging strategy which enables the dynamic alteration of colony demography in response to internal and external conditions. The strategy is likely key to the ability of M. pharaonis and similar ants to thrive in disturbed habitats and to become widespread invasive species.\n\nSignificance StatementThe defining feature of social insect societies is the presence of alternate queen (reproductive) and worker (non-reproductive) castes of individuals. The fitness of social insect colonies is dependent upon efficient allocation of resources to alternate castes, particularly in the case of highly polygynous (multi-queen) societies. However, the mechanisms by which such societies regulate caste allocation are largely unknown. In this study, we show that colonies manipulate their production of queens (and also males) versus workers according to the present density of eggs in the colony, which serves as a reliable indicator of queens fertility. Provided egg density is high, colonies kill queen-and male-destined larvae; when egg density falls, colonies begin to rear queens and males. This flexible resource allocation strategy is key to the ability of highly polygynous species to thrive in marginal (often human-associated) habitats.

ecology↗