Biology subjects

Abouheif, E.

Publications and source records attributed to Abouheif, E..

7 recordsLinked to original sources

bioRxiv2025

Latent gene network expression underlies the reversion of a polyphenic trait in the worker caste of ants

Polyphenisms--where alternative phenotypes develop from a single genome in response to environmental cues--are not only widespread in nature, but also occur at multiple levels of biological organization, from cells to individuals to societies. Polyphenism is thought to promote phenotypic diversification through the gain, loss, and re-evolution of alternative phenotypes. After the origin of a polyphenism, one of the alternative phenotypes often retains the developmental capacity to produce the ancestral trait, thereby permitting the other to evolve rapidly. Yet, little is known about the developmental processes underlying the re-evolution of polyphenic traits and how they may produce phenotypic diversification. Here we address this question by focusing on the caste polyphenism in ant societies, which produces a winged queen caste and a wingless worker caste in a single colony in response to environmental cues. We show, in a hyperdiverse group of ants, that a caste-specific trait called the ocelli (3 simple eyes on the dorsal head) is always present across queen castes but was lost and partially re-evolved multiple times, giving rise to novel patterns (1 ocelli) in the worker castes. Surprisingly, we discovered that a hidden (latent) expression of the ocelli gene regulatory network in worker castes that lost ocelli underlies the partial re-evolution of ocelli in this group. We therefore propose that latent developmental potentials may generally persist across polyphenic systems, including ant castes, and may facilitate the partial re-evolution of novel phenotypic patterns.

evolutionary biology↗

bioRxiv2024

Thrifty superorganism phenotypes emerge as a plastic response to extreme environments in the Hercules ant

AO_SCPLOWBSTRACTC_SCPLOWAdaptation to extreme environments is commonly assumed to occur through microevolutionary change. However, studies of high-altitude human populations show that organisms can also respond to nutritional stress through developmental plasticity, producing thrifty phenotypes that prioritize essential function over costly structures. Whether this adaptive strategy extends beyond humans, and how it operates in natural systems, remains largely unexplored. Here, we test the thrifty phenotype hypothesis (TPH) in a widely distributed superorganism, the carpenter ant Camponotus herculeanus, which inhabits some of the most environmentally challenging regions of the Northern Hemisphere. Colonies comprise inexpensive minor workers and energetically costly major workers, providing a powerful system for examining plastic investment under resource limitation. We quantified relationships between caste structure and climate and conducted a common-garden experiment to test the TPH. We show that the proportion of major workers declines with increasing latitude, independently of body size and colony size, and is best predicted by the number of days, annually, during which workers can nurse brood. Experimental results further demonstrate that colonies rapidly and plastically adjust caste structure in response to environmental conditions. Our findings reveal that thrifty phenotypes can emerge in superorganisms and could represent a conserved developmental response to environmental stress. By extending a central hypothesis from human biology to social insects, this work provides a unifying framework for understanding how developmental plasticity shapes adaptation across levels of biological organization.

ecology↗

bioRxiv2024

Inferring a role for programmed cell death during the origin and evolution of wing polyphenism in ants

Major evolutionary transitions in individuality occur when solitary individuals unite to form a single replicating organism with a division of labor between constituent individuals. Key examples include the evolution of multicellularity, eusociality, and obligate endosymbiosis. Programmed Cell Death (PCD) has been proposed to play an important role during major transitions to multicellularity, yet it remains unclear to what extent PCD plays a role in other major transitions. Here we test if PCD was involved in the major transition to eusociality in ants, where solitary individuals united to form eusocial colonies with a division of labor between a winged queen caste and a wingless worker caste. The development of wings in queens but not in workers in response to environmental cues is called wing polyphenism, which evolved once and is a general feature of ants. Both wing polyphenism and eusociality evolved at the same time during the origin of ants and were likely intimately linked--the suppression of wings in workers may have reduced their ability to participate in mating flights thereby reinforcing the reproductive division of labor within the parental nest. We therefore tested whether PCD plays a role in the degeneration of wings during development of the worker caste across the ant phylogeny encompassing species with both ancestral-like and derived characteristics. We show that PCD, mediated by the apoptosis pathway, is present in the degenerating wing primordia of worker larvae in 15 out of the 16 species tested. Using ancestral state reconstruction, we infer a role for PCD in regulating wing polyphenism in the last common ancestor of all extant ants. Our findings provide evidence that a degenerative mechanism (PCD) plays a role in the origin of wing polyphenism, and therefore, in facilitating the major transition to eusociality in ants. PCD may generally play a key role in the evolution of biological complexity by facilitating major transitions at different scales, such as multicellularity and eusociality.

evolutionary biology↗

bioRxiv2023

Embryogenesis in myrmicine ants combines features of short and long germ-band modes of development

Ants exhibit complex social organization, morphologically distinct castes with division of labor, and the exploitation of diverse ecological niches. The extent to which these features have influenced embryonic development relative to other insects remains unclear. Insect embryogenesis has been classified into one of three modes: long, short, and intermediate germ-band. In long germ-band development, exemplified by the fruit fly Drosophila melanogaster, segments along the entire anterior-posterior axis of the embryonic primordium are established almost simultaneously, prior to gastrulation, with the initial embryonic primordium surrounding almost the entire volume of the egg. In short and intermediate germ-band modes, the embryonic primordium occupies a smaller proportion of the egg surface, with anterior segments initially specified, and remaining segments being added sequentially from a posterior growth zone. Here, we show a novel pattern of development in three myrmicine ants, the fungus-gardening ants Atta texana and Mycocepurus smithii, and the red imported fire ant Solenopsis invicta. Early in embryogenesis, they exhibit features of short germ-band development, while later in development they exhibit a newly-characterized progressive pattern of segmentation that has been associated with some long germ-band-developing insects. Moreover, despite similarities in the size of ant and Drosophila eggs, the duration of embryogenesis in the three ant species is 10 to 20-fold longer than in Drosophila and is also significantly longer than in the honeybee Apis mellifera and the jewel wasp Nasonia vitripennis. In addition, the embryos produced by A. texana foundress queens develop to first instar larvae 25% faster than embryos produced by mature queens. We discuss these results in the context of the eusocial lifestyle of ants.

developmental biology↗

bioRxiv2021

Nano-CT characterization reveals coordinated growth of a rudimentary organ necessary for soldier development in the ant Pheidole hyatti

The growth of imaginal discs in holometabolous insects is coordinated with larval growth to ensure the symmetrical and proportional development of the adult appendages. In ants, the differential growth of these discs generates distinct castes - the winged male and queen castes and the wingless worker caste. In the hyperdiverse ant genus Pheidole, the worker caste is composed of two morphologically distinct subcastes: small minor workers and larger, big-headed soldiers. Although these worker subcastes are completely wingless, soldier larvae develop rudimentary forewing discs that are necessary for generating the disproportionate head-to-body scaling of the big-headed soldier subcaste. However, it remains unclear whether rudimentary forewing discs in soldier larvae are coordinated with other imaginal discs, and whether disc growth and coordination patterns vary between the minor worker and soldier subcastes. Here we show, using quantitative nano-CT three-dimensional analyses, that growth of the soldier rudimentary forewing discs is coordinated with the increase in volume of the leg and eye-antennal (head) discs as well as with larval size. We found that the growth rate of the rudimentary forewing discs differs from the leg discs but is similar to the growth of the head (eye-antennal) discs relative to larval size, suggesting that growth of each type of imaginal disc may be differentially regulated. In addition to their larger size, the soldier eye-antennal discs increase in width as they undergo morphogenesis to generate the characteristic shape of the large soldier head, suggesting that the rudimentary forewing discs may regulate their patterning in addition to their growth. Finally, we observe little growth of the leg and eye-antennal discs during the bipotential stage, while in minor worker development these discs grow at similar rates to one another in coordination with larval size to generate the smaller minor worker subcaste. Our results suggest that rudimentary organs with regulatory functions may participate in new patterns of inter-organ coordination and regulation to produce novel phenotypes and complex worker caste systems. We provide characterization of larval development and imaginal disc growth and morphogenesis with the aim of highlighting this as an emerging system for the study of rudimentary organs during development and evolution.

developmental biology↗

bioRxiv2020

From egg to adult: a developmental table of the ant Monomorium pharaonis

Ants are one of the most ecologically and evolutionarily successful groups of animals and exhibit a remarkable degree of phenotypic diversity. This success is largely attributed to the fact that all ants are eusocial and live in colonies with a reproductive division of labor between morphologically distinct queen and worker castes. Yet, despite over a century of studies on caste determination and evolution in ants, we lack a complete ontogenetic series from egg to adult for any ant species. We therefore present a developmental table for the Pharaoh ant Monomorium pharaonis, a species whose colonies simultaneously produce both reproductive queens and completely sterile workers. In total, M. pharaonis embryonic, larval, and pupal development lasts 45 days. During embryogenesis, the majority of developmental events are conserved between M. pharaonis and the fruit fly Drosophila melanogaster. However, we discovered two types of same-stage embryos prior to gastrulation: (1) embryos with internalized germ cells; and (2) embryos with germ cells outside of the blastoderm at the posterior pole. Moreover, we found two-types of embryos following germ band extension: (1) fertile embryos with primordial germ cells; and (2) sterile embryos with no germ cells. Together, our data shows that the queen (fertile) and worker (sterile) phenotypes are already determined and differentiated by early embryogenesis. During larval development, previous studies and our data find 3 larval instars reproductives and workers. However, there is considerable variation within each caste-specific instar, making it difficult to lineate instar boundaries. Here, we propose that developmental and anatomical markers can segregate larvae into gyne (unmatted queen), male and worker castes, including during the 1st larval instar. Overall, we hope that the ontogenetic series we present here will serve as a blueprint for the generation of future ant developmental tables.

developmental biology↗

bioRxiv2018

The genome of the water strider Gerris buenoi reveals expansions of gene repertoires associated with adaptations to life on the water

The semi-aquatic bugs conquered water surfaces worldwide and occupy ponds, streams, lakes, mangroves, and even open oceans. As such, they inspired a range of scientific studies from ecology and evolution to developmental genetics and hydrodynamics of fluid locomotion. However, the lack of a representative water strider genome hinders thorough investigations of the mechanisms underlying the processes of adaptation and diversification in this group. Here we report the sequencing and manual annotation of the Gerris buenoi (G. buenoi) genome, the first water strider genome to be sequenced so far. G. buenoi genome is about 1 000Mb and the sequencing effort recovered 20 949 predicted protein-coding genes. Manual annotation uncovered a number of local (tandem and proximal) gene duplications and expansions of gene families known for their importance in a variety of processes associated with morphological and physiological adaptations to water surface lifestyle. These expansions affect key processes such as growth, vision, desiccation resistance, detoxification, olfaction and epigenetic components. Strikingly, the G. buenoi genome contains three Insulin Receptors, a unique case among metazoans, suggesting key changes in the rewiring and function of the insulin pathway. Other genomic changes include wavelength sensitivity shifts in opsin proteins likely in association with the requirements of vision in water habitats. Our findings suggest that local gene duplications might have had an important role during the evolution of water striders. These findings along with the G. buenoi genome open exciting research opportunities to understand adaptation and genome evolution of this unique hemimetabolous insect.

genomics↗