Reproductive Competition in Multiple-queen Fire Ant Colonies: Insights from Analyses of Breeding Systems

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The paper characterizes breeding systems in invasive fire ant Solenopsis invicta, focusing on how a supergene determines whether colonies are monogyne (single queen) or polygyne (multiple queens). Using a large longitudinal semi-natural experiment, the authors track parentage, relatedness, and supergene genotype, and they also reanalyze data from prior studies to show that polygyne colonies have highly variable queen number, queens generally mate once, and nestmate breeders (queens and their mates) are unrelated, with pervasive reproductive skew, especially among sexual daughters. Paternity skew is pronounced and stable, and uncommon polyandry is linked to queens remating after initial mating with males carrying the Sb supergene haplotype, which is associated with low sperm counts. The authors note that many features of the polygyne-form breeding system remain uncharacterized, limiting full resolution. The paper does not explicitly discuss endometriosis or adenomyosis; it was included in the corpus via a keyword match in the upstream search index.

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Abstract

When animals reproduce in social groups, the potential for conflict and cooperation is shaped by the number of reproductive individuals (breeders), their relatedness to one another, and division of reproduction among them. These features comprise species’ “breeding systems.” Despite their importance, breeding systems are poorly characterized in most social animals, and detailed accounts for single species are rare. Here, we fully characterize the breeding systems in invasive populations of the fire ant Solenopsis invicta, a species in which a large genetic element (supergene) determines whether a colony has a single queen (monogyne social form) or multiple queens (polygyne form). Colonies of the monogyne form are simple families, and the breeding system is correspondingly straightforward. The breeding system of the polygyne form is complex, with many features still uncharacterized. We conducted a large longitudinal experiment tracking parentage, relatedness, and supergene genotype in semi-natural polygyne colonies. Along with reanalyzed data from previous studies, we show that colony queen number is highly variable, queens generally mate once, nestmate breeders (queens and their mates) are unrelated, and reproductive skew is pervasive, especially for sexual daughters. Uncommon instances of polyandry occur when a queen remates after initially mating with a male bearing the Sb supergene haplotype (associated with low sperm counts). Paternity skew is pronounced and stable, with Sb sperm contributing to a minority of offspring (particularly sexuals). Thus, the supergene not only determines colony queen number, it broadly affects the breeding system, with impacts on colony kin structure and opportunities for reproductive competition.
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Reproductive Competition in Multiple-queen Fire Ant Colonies: Insights from Analyses of Breeding Systems | Authorea try { document.documentElement.classList.add('js'); } catch (e) { } var _gaq = _gaq || []; _gaq.push(['_setAccount', 'G-8VDV14Y67G']); _gaq.push(['_trackPageview']); (function() { var ga = document.createElement('script'); ga.type = 'text/javascript'; ga.async = true; ga.src = ('https:' == document.location.protocol ? 'https://ssl' : 'http://www') + '.google-analytics.com/ga.js'; var s = document.getElementsByTagName('script')[0]; s.parentNode.insertBefore(ga, s); })(); Skip to main content Preprints Collections Wiley Open Research IET Open Research Ecological Society of Japan All Collections About About Authorea FAQs Contact Us Quick Search anywhere Search for preprint articles, keywords, etc. Search Search ADVANCED SEARCH SCROLL This is a preprint and has not been peer reviewed. Data may be preliminary. 18 March 2025 V1 Latest version Share on Reproductive Competition in Multiple-queen Fire Ant Colonies: Insights from Analyses of Breeding Systems Authors : Sierra Hale Walker , Kip Lacy , Kenneth Ross , and Haolin Zeng 0000-0002-9921-7335 [email protected] Authors Info & Affiliations https://doi.org/10.22541/au.174229826.68677306/v1 341 views 123 downloads Contents Abstract Supplementary Material Information & Authors Metrics & Citations View Options References Figures Tables Media Share Abstract When animals reproduce in social groups, the potential for conflict and cooperation is shaped by the number of reproductive individuals (breeders), their relatedness to one another, and division of reproduction among them. These features comprise species’ “breeding systems.” Despite their importance, breeding systems are poorly characterized in most social animals, and detailed accounts for single species are rare. Here, we fully characterize the breeding systems in invasive populations of the fire ant Solenopsis invicta, a species in which a large genetic element (supergene) determines whether a colony has a single queen (monogyne social form) or multiple queens (polygyne form). Colonies of the monogyne form are simple families, and the breeding system is correspondingly straightforward. The breeding system of the polygyne form is complex, with many features still uncharacterized. We conducted a large longitudinal experiment tracking parentage, relatedness, and supergene genotype in semi-natural polygyne colonies. Along with reanalyzed data from previous studies, we show that colony queen number is highly variable, queens generally mate once, nestmate breeders (queens and their mates) are unrelated, and reproductive skew is pervasive, especially for sexual daughters. Uncommon instances of polyandry occur when a queen remates after initially mating with a male bearing the Sb supergene haplotype (associated with low sperm counts). Paternity skew is pronounced and stable, with Sb sperm contributing to a minority of offspring (particularly sexuals). Thus, the supergene not only determines colony queen number, it broadly affects the breeding system, with impacts on colony kin structure and opportunities for reproductive competition. Supplementary Material File (breeding system_main text_mar17.docx) Download 4.08 MB Information & Authors Information Version history V1 Version 1 18 March 2025 Copyright This work is licensed under a Non Exclusive No Reuse License. Keywords animal mating/breeding systems genetic conflict polyandry reproductive skew social organization supergene Authors Affiliations Sierra Hale Walker University of Georgia View all articles by this author Kip Lacy The Rockefeller University View all articles by this author Kenneth Ross University of Georgia View all articles by this author Haolin Zeng 0000-0002-9921-7335 [email protected] University of Georgia View all articles by this author Metrics & Citations Metrics Article Usage 341 views 123 downloads .FvxKWukQNSOunydq8rnd { width: 100px; } Citations Download citation Sierra Hale Walker, Kip Lacy, Kenneth Ross, et al. Reproductive Competition in Multiple-queen Fire Ant Colonies: Insights from Analyses of Breeding Systems. Authorea . 18 March 2025. DOI: https://doi.org/10.22541/au.174229826.68677306/v1 If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. 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