Hale Walker Sierra, Lacy Kip D, Ross Kenneth G, Zeng Haolin
Department of Entomology University of Georgia Athens Georgia USA.
Laboratory of Social Evolution and Behavior The Rockefeller University New York New York USA.
Ecol Evol. 2025 Aug 25;15(8):e71888. doi: 10.1002/ece3.71888. eCollection 2025 Aug.
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 comprehensively characterize the breeding systems of the fire ant , an invasive 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 not well characterized. We conducted a large longitudinal experiment tracking parentage, relatedness, and supergene genotype in laboratory-reared 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) generally are unrelated, and reproductive skew is pervasive, especially for parentage of sexual daughters. Uncommon instances of polyandry occur when a queen remates after initially mating with a male bearing the supergene haplotype (associated with small size and low sperm counts). Paternity skew is pronounced and stable, with sperm contributing to a minority of offspring (particularly sexual daughters) of polyandrous queens. The supergene thus not only determines colony queen number, it broadly affects the breeding system, impacting colony kin structure and setting the stage for conflict and cooperation in the colony. This study can serve as a template for studies of the constellation of factors that affect group genetic structure in other social animals.
当动物在社会群体中繁殖时，冲突与合作的可能性受到繁殖个体（繁殖者）的数量、它们彼此之间的亲缘关系以及它们之间的繁殖分工的影响。这些特征构成了物种的“繁殖系统”。尽管繁殖系统很重要，但在大多数社会性动物中，其特征描述并不充分，对单一物种的详细描述也很少见。在这里，我们全面描述了火蚁的繁殖系统，火蚁是一种入侵物种，其中一个大型遗传元件（超级基因）决定了蚁群是只有一个蚁后（单蚁后社会形态）还是有多个蚁后（多蚁后形态）。单蚁后形态的蚁群是简单的家族，其繁殖系统相应地也很简单直接。多蚁后形态的繁殖系统很复杂，许多特征仍未得到很好的描述。我们进行了一项大型纵向实验，追踪实验室饲养的多蚁后蚁群中的亲子关系、亲缘关系和超级基因基因型。结合对先前研究数据的重新分析，我们发现蚁群中的蚁后数量高度可变，蚁后通常只交配一次，同巢的繁殖者（蚁后及其配偶）通常没有亲缘关系，繁殖偏斜普遍存在，尤其是在有性雌性后代的亲子关系方面。当蚁后最初与携带超级基因单倍型（与体型小和精子数量少相关）的雄性交配后再次交配时，会出现罕见的一妻多夫情况。父权偏斜明显且稳定，精子对一妻多夫蚁后的少数后代（尤其是有性雌性后代）有贡献。因此，超级基因不仅决定了蚁群中的蚁后数量，还广泛影响繁殖系统，影响蚁群的亲属结构，并为蚁群中的冲突与合作奠定基础。这项研究可以作为研究影响其他社会性动物群体遗传结构的一系列因素的模板。
