Recurring adaptive introgression of a supergene that determines social organization

Introgression has been proposed as an essential source of trait adaptation. However, a key barrier to adaptive introgression is that recombination can break down combinations of alleles that underpin many traits. Supergene regions, where suppressed recombination leads to joint inheritance of alleles at many loci, could overcome this challenge. Here, we study the evolution of a large supergene region that determines a major social and ecological trait in Solenopsis fire ants: whether colonies have one queen or multiple queens. Using coalescent-based phylogenies built from the genomes of 365 haploid fire ant males, we show that the supergene variant responsible for multiple-queen colonies evolved in one species and repeatedly spread to other species through introgressive hybridization. This finding highlights how supergene architecture can enable a complex adaptive phenotype to recurrently permeate species boundaries.

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Alternative Genetic Foundations for a Key Social Polymorphism in Fire Ants

Genetics ◽

10.1093/genetics/165.4.1853 ◽

2003 ◽

Vol 165 (4) ◽

pp. 1853-1867

Author(s):

Kenneth G Ross ◽

Michael J B Krieger ◽

D DeWayne Shoemaker

Keyword(s):

Amino Acid ◽

Social Organization ◽

Allelic Variation ◽

Major Gene ◽

Fire Ants ◽

Fire Ant ◽

Gene Frequencies ◽

Specific Amino Acid ◽

Social Polymorphism ◽

In Fire

Abstract Little is known about the genetic foundations of colony social organization. One rare example in which a single major gene is implicated in the expression of alternative social organizations involves the presumed odorant-binding protein gene Gp-9 in fire ants. Specific amino acid substitutions in this gene invariably are associated with the expression of monogyny (single queen per colony) or polygyny (multiple queens per colony) in fire ant species of the Solenopsis richteri clade. These substitutions are hypothesized to alter the abilities of workers to recognize queens and thereby regulate their numbers in a colony. We examined whether these same substitutions underlie the monogyny/polygyny social polymorphism in the distantly related fire ant S. geminata. We found that Gp-9 coding region sequences are identical in the polygyne and monogyne forms of this species, disproving our hypothesis that one or a few specific amino acid replacements in the protein are necessary to induce transitions in social organization in fire ants. On the other hand, polygyne S. geminata differs genetically from the monogyne form in ways not mirrored in the two forms of S. invicta, a well-studied member of the S. richteri clade, supporting the conclusion that polygyny did not evolve via analogous routes in the two lineages. Specifically, polygyne S. geminata has lower genetic diversity and different gene frequencies than the monogyne form, suggesting that the polygyne form originated via a founder event from a local monogyne population. These comparative data suggest an alternative route to polygyny in S. geminata in which loss of allelic variation at genes encoding recognition cues has led to a breakdown in discrimination abilities and the consequent acceptance of multiple queens in colonies.

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Comparative Immature Morphology of Brazilian Fire Ants (Hymenoptera: Formicidae:Solenopsis)

Psyche A Journal of Entomology ◽

10.1155/2012/183284 ◽

2012 ◽

Vol 2012 ◽

pp. 1-10 ◽

Cited By ~ 2

Author(s):

Eduardo Gonçalves Paterson Fox ◽

Daniel Russ Solis ◽

Mônica Lanzoni Rossi ◽

Jacques Hubert Charles Delabie ◽

Rodrigo Fernando de Souza ◽

...

Keyword(s):

Intraspecific Variation ◽

Solenopsis Invicta ◽

Morphological Traits ◽

Species Level ◽

Fire Ants ◽

Fire Ant ◽

Solenopsis Geminata ◽

Body Dimensions ◽

Larval Instars ◽

Genus Level

Although common in Brazil, the biology of the fire antSolenopsis saevissima(Smith) is still poorly studied. Larval descriptions are useful to genus-level ant systematics and sometimes to species-level taxonomy. This study presents a detailed description of juveniles ofS. saevissimafrom Brazil, which were compared with Brazilian specimens ofSolenopsis invictaBuren,Solenopsis geminata(Fabricius), andSolenopsis altipunctataPitts. Different larval instars were separated by diagnostic morphological traits which were confirmed by observing moults. Reproductive larvae could be easily sorted by their distinctive body dimensions and shape. Contrary to previous reports on this species, the larvae ofS. saevissimaproved to be generally identical to those ofS. invicta, while a few specimens resembled those of other close species, such asSolenopsis megergatesTrager. Mature larvae thus presented considerable intraspecific variation in some characters recently proposed to aid fire ant species separation (morphology of head hairs).

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Distinct colony boundaries and larval discrimination in polygyne red imported fire ants (Solenopsis invicta)

10.22541/au.163251827.70085127/v1 ◽

2021 ◽

Author(s):

MacKenzie Kjeldgaard ◽

Pierre-André Eyer ◽

Collin McMichael ◽

Alison Bockoven ◽

Joanie King ◽

...

Keyword(s):

Solenopsis Invicta ◽

Sucrose Solution ◽

Ecological Impact ◽

Egg Laying ◽

Fire Ants ◽

Fire Ant ◽

Red Imported Fire Ant ◽

Invasive Ant ◽

Nestmate Discrimination ◽

Social Forms

Evaluating the factors that promote invasive ant abundance is critical to assess their ecological impact and inform their management. Many invasive ant species show reduced nestmate recognition and an absence of boundaries between unrelated nests, which allow populations to achieve greater densities due to reduced intraspecific competition. We examined nestmate discrimination and colony boundaries in introduced populations of the red imported fire ant (Solenopsis invicta; hereafter, fire ant). Fire ants occur in two social forms: monogyne (colonies with a single egg-laying queen) and polygyne (colonies with multiple egg-laying queens). In contrast with monogyne nests, polygyne nests are thought to be interconnected due to the reduced antagonism between non-nestmate polygyne workers, perhaps because polygyne workers habituate the colony to an odor unique to Gp-9-carrying adults. However, colony boundaries and nestmate discrimination are poorly documented, particularly for worker-brood interactions. To delimit boundaries between field colonies, we correlated the exchange of a N-glycine tracer dissolved in a sucrose solution with social form. We also evaluated nestmate discrimination between polygyne workers and larvae in the laboratory. Counter to our expectations, polygyne colonies behaved identically to monogyne colonies, suggesting both social forms maintain strict colony boundaries. Polygyne workers also preferentially fed larval nestmates and may have selectively cannibalized non-nestmates. The levels of relatedness among workers in polygyne colonies was higher than those previously reported in North America (mean ±SE: 0.269 ± 0.037). Our study highlights the importance of combining genetic analyses with direct quantification of resource exchange to better understand the factors influencing ant invasions.

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Genomic architecture and evolutionary antagonism drive allelic expression bias in the social supergene of red fire ants

eLife ◽

10.7554/elife.55862 ◽

2020 ◽

Vol 9 ◽

Author(s):

Carlos Martinez-Ruiz ◽

Rodrigo Pracana ◽

Eckart Stolle ◽

Carolina Ivon Paris ◽

Richard A Nichols ◽

...

Keyword(s):

Fire Ants ◽

Allelic Expression ◽

Body Parts ◽

Adaptive Responses ◽

Social Forms ◽

Complex Phenotypes ◽

The Social ◽

Expression Bias ◽

Allelic Differences ◽

Suppressed Recombination

Supergene regions maintain alleles of multiple genes in tight linkage through suppressed recombination. Despite their importance in determining complex phenotypes, our empirical understanding of early supergene evolution is limited. Here we focus on the young ‘social’ supergene of fire ants, a powerful system for disentangling the effects of evolutionary antagonism and suppressed recombination. We hypothesize that gene degeneration and social antagonism shaped the evolution of the fire ant supergene, resulting in distinct patterns of gene expression. We test these ideas by identifying allelic differences between supergene variants, characterizing allelic expression across populations, castes and body parts, and contrasting allelic expression biases with differences in expression between social forms. We find strong signatures of gene degeneration and gene-specific dosage compensation. On this background, a small portion of the genes has the signature of adaptive responses to evolutionary antagonism between social forms.

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Balancing selection and introgression of newt immune-response genes

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2018.0819 ◽

2018 ◽

Vol 285 (1884) ◽

pp. 20180819 ◽

Cited By ~ 7

Author(s):

Anna Fijarczyk ◽

Katarzyna Dudek ◽

Marta Niedzicka ◽

Wiesław Babik

Keyword(s):

Gene Flow ◽

Genetic Variants ◽

Balancing Selection ◽

Species Boundaries ◽

Adaptive Introgression ◽

Interspecific Introgression ◽

Differential Gene ◽

And Migration ◽

Relevant Variation ◽

Novel Allele

The importance of interspecific introgression as a source of adaptive variation is increasingly recognized. Theory predicts that beneficial genetic variants cross species boundaries easily even when interspecific hybridization is rare and gene flow is strongly constrained throughout the genome. However, it remains unclear whether certain classes of genes are particularly prone to adaptive introgression. Genes affected by balancing selection (BS) may constitute such a class, because forms of BS that favour novel, initially rare alleles, should facilitate introgression. We tested this hypothesis in hybridizing newts by comparing 13 genes with signatures of BS, in particular an excess of common non-synonymous polymorphisms, to the genomic background (154 genes). Parapatric hybridizing taxa were less differentiated in BS candidate genes than more closely related allopatric lineages, while the opposite was observed in the control genes. Coalescent and forward simulations that explored neutral and BS scenarios under isolation and migration showed that processes other than differential gene flow are unlikely to account for this pattern. We conclude that BS, probably involving a form of novel allele advantage, promotes introgression. This mechanism may be a source of adaptively relevant variation in hybridizing species over prolonged periods.

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Near Fatal Fire Ant Envenomation of a Newborn

PEDIATRICS ◽

10.1542/peds.90.4.622 ◽

1992 ◽

Vol 90 (4) ◽

pp. 622-624

Author(s):

WILLUAM E. HARDWICK ◽

JAMES A. ROYALL ◽

BRUCE A. PETITT ◽

SAMUEL J. TILDEN

Keyword(s):

Solenopsis Invicta ◽

Fire Ants ◽

Fire Ant ◽

Port City ◽

Southern States ◽

South Central ◽

Solenopsis Richteri ◽

Central United States ◽

Imported Fire Ants ◽

Venom Hypersensitivity

Imported fire ants, Solenopsis richteri and Solenopsis invicta, are menacing health hazards for the 20 to 30 million people who live in the fire ant-infested regions of the southeastern and south central United States. In the early 1900s, fire ants were brought into the port city of Mobile, Alabama, on vegetation and produce from South America. Their aggressive behavior compared to native ants and the favorable climate throughout the southeast allowed extensive spread. In 1985 it was estimated that fire ants infested approximately 250 million acres in eleven southern states and Puerto Rico.1 In infested areas fire ants account for 90% of all ant populations and stings from fire ants are more frequent than stings from other hymenoptera, becoming the most common cause of insect venom hypersensitivity.

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Hymenopteran Pests: Family Formicidae

Turfgrass Insects of the United States and Canada ◽

10.7591/cornell/9781501747953.003.0020 ◽

2020 ◽

pp. 317-331

Author(s):

Patricia J. Vittum

Keyword(s):

United States ◽

Sandy Soils ◽

The United States ◽

Fire Ants ◽

Fire Ant ◽

Red Imported Fire Ant ◽

The Many ◽

Surrounding Areas ◽

Water Holding ◽

Imported Fire Ant

This chapter explores the many species of ants, order Hymenoptera, family Formicidae, which invade turfgrass areas throughout the United States. The subfamily Formicinae includes many ants found on turf. The fire ants are by far the most important and common pest ants of turfgrass in the southeastern states. Ants are primarily troublesome in turfgrass areas because they build mounds as they form subterranean homes for their colonies. They seek out drier, well-drained sandy soils that have low water-holding capacity. The galleries they form, which damage roots, add to the desiccation of the soil, and the turf in the surrounding areas becomes thin and unsightly. Mounds of various sizes and shapes, formed according to the habits of the ant species, are often detrimental to mower blades. The chapter then looks at the red imported fire ant, the turfgrass ant, and the harvester ant.

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Naturally Occurring Compounds/Materials as Alternatives to Synthetic Chemical Insecticides for Use in Fire Ant Management

Insects ◽

10.3390/insects11110758 ◽

2020 ◽

Vol 11 (11) ◽

pp. 758

Author(s):

Jian Chen ◽

David H. Oi

Keyword(s):

Solenopsis Invicta ◽

Fire Ants ◽

Fire Ant ◽

Red Imported Fire Ant ◽

Natural Toxins ◽

Naturally Occurring ◽

Solenopsis Invicta Buren ◽

In Fire ◽

Imported Fire Ant ◽

Made In

The invasive red imported fire ant, Solenopsis invicta Buren (hereafter, fire ants), is a significant threat to public health and a danger to livestock, pets and wildlife due to their venomous stings. The fire ant has invaded many countries and regions and has become a globally significant pest. The current major tool to manage fire ants are synthetic insecticides that are used largely as stomach poisons in bait products or contact insecticides in spray, broadcast, drench, and dust products for area and nest treatments. In addition to these insecticide products, repellants and fumigants can also be useful in some unique scenarios. The ever-increasing public concern about the potential adverse effects of synthetic insecticides on health and the environment has been a driving force for searching for safer alternatives to control fire ants. Tremendous effort has been made in developing biologically-based control for managing fire ants; however, natural products continue to be one of the most attractive sources of safe alternatives to synthetic insecticides. Here, we summarized the synthetic insecticides that are currently used in managing fire ants, available alternative products in the current market, and academic efforts in searching for fire ant natural toxins, repellants and fumigants.

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History of predator exposure affects cell-mediated immunity in female eastern fence lizards, Sceloporus undulatus (Squamata: Phrynosomatidae)

Biological Journal of the Linnean Society ◽

10.1093/biolinnean/blz154 ◽

2019 ◽

Author(s):

Kristen Sprayberry ◽

Catherine Tylan ◽

Dustin A S Owen ◽

Kirsty J Macleod ◽

Michael J Sheriff ◽

...

Keyword(s):

Immune Response ◽

Evolutionary History ◽

Fire Ants ◽

Fire Ant ◽

Cell Mediated Immunity ◽

Sceloporus Undulatus ◽

Environmental Threats ◽

Dosing Regimens ◽

History Of ◽

Corticosterone Treatment

Abstract On exposure to stressors, energy is diverted from non-urgent functions towards those important for immediate survival. The degree and nature of reallocation may be affected by the evolutionary history of the animal. The eastern fence lizard (Sceloporus undulatus) coexists in parts of its range with invasive fire ants (Solenopsis invicta), which attack and wound lizards and elevate stress-relevant hormones (corticosterone), whereas other populations have never been exposed to fire ants. We examined how a history of fire ant invasion affected the immune response in female lizards after exposure to exogenous corticosterone (mimicking exposure to a stressor) during gestation (dosing regimens differed among corticosterone-exposed lizards owing to the constraints of the original studies, but we found no evidence that this affected the outcome of the present study). A history of exposure to predatory stressors (fire ants) and corticosterone treatment affected cell-mediated immunity. Lizards from fire ant-invaded sites had a reduced immune response compared with those from uninvaded sites. Corticosterone treatment had no effect on the immune response of lizards from invaded sites but reduced the immune response of lizards from uninvaded sites. This suggests that an evolutionary history of exposure to wounding alters the immune response to corticosterone. Future work on how the immune system responds to environmental threats will be informative for the prediction and management of these threats.

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Identification of Key Genes for the Precise Classification between Solenopsis invicta and S. geminata Facilitating the Quarantine Process

Genes ◽

10.3390/genes10100812 ◽

2019 ◽

Vol 10 (10) ◽

pp. 812 ◽

Cited By ~ 1

Author(s):

Kil-Hyun Kim ◽

Ji-Su Kim ◽

Hyun-Ji Cho ◽

Jong-Ho Lee ◽

Tae-Hwan Jun ◽

...

Keyword(s):

Solenopsis Invicta ◽

Environmental Safety ◽

Fire Ants ◽

Fire Ant ◽

Whole Genome Sequence ◽

Red Imported Fire Ant ◽

Caps Marker ◽

Invasive Exotic Species ◽

Invasive Exotic ◽

First Time

One of the 100 worst invasive exotic species, Solenopsis invicta (red imported fire ant), has the possibility to induce an allergic reaction that may eventually cause death from its aggressive stinging. In 2017, S. invicta was found at a container yard in Gamman Port, Busan, South Korea for the first time. It may result in an infestation of fire ants in the Korean environment. After this incident, sensitive quarantine procedures are required to detect possible contamination of fire ants in imported containers. However, currently, fire ant identification relies on phenotypic characteristics. This requires highly trained experts for identification and there are not enough to cover all imported containers. Here, we develop a key molecular marker to distinguish S. invicta from others using the whole genome sequence (WGS) of collected S. invicta from Gamman Port and NCBI-deposited WGS data of S.invicta and S. geminata. The consolidated genotypes of Solenopsis genus successfully indicate the distinguishable gene. The gel-based experimental validation confirmed expected classification and the developed cleaved amplified polymorphic sequences (CAPS) marker also gave a consistent result. Using the CAPS marker derived from our consolidated genotypes, the samples collected from containers in several ports can be easily tested by PCR in a few hours. The quick and easy test would increase not only the labor efficiency but also the environmental safety from fire ants.

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