Joint Evolution of Asexuality and Queen Number in an Ant

• Published in: Current biology Vol. 29; no. 8; pp. 1394 - 1400.e4
• Main Authors: Lacy, Kip D., Shoemaker, DeWayne, Ross, Kenneth G.
• Format: Journal Article
• Language: English
• Published: England Elsevier Ltd 22-04-2019
• Subjects: Animals; ants; Ants - physiology; Biological Evolution; facultative asexuality; Female; fire ants; genetic caste determination; Male; mating systems; parthenogenesis; polygyny; Reproduction; Social Behavior; social hybridogenesis; social polymorphism; Solenopsis geminata; ants; parthenogenesis; polygyny; facultative asexuality; genetic caste determination; fire ants; social polymorphism; mating systems; social hybridogenesis; Solenopsis geminata
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2019.03.018

Ants exhibit a striking diversity of reproductive systems, varying in traits such as the number of reproductives per colony [1], the mode of daughter production (sexual or asexual) [2], and the mode of caste determination (genetic or environmental) [3]. Species employing mixed reproductive systems present a unique opportunity to explore the causes and consequences of alternative breeding strategies. Mixed reproductive systems in ants include social polymorphism in colony queen number, whereby single-queen (monogyne) and multiple-queen (polygyne) colonies co-occur within species [4–7], and facultative asexuality, in which female offspring may be produced sexually or asexually within colonies [8–13]. Here, we document a remarkable confluence of multiple mixed reproductive systems in the tropical fire ant, Solenopsis geminata, in a population with three important features: (1) polygyne colonies produce workers sexually but queens asexually, whereas monogyne colonies produce both castes sexually; (2) polygyne queens mate with monogyne males to produce workers, but monogyne queens do not mate with polygyne males; and (3) different asexual/polygyne lineages evidently were founded separately by genetically distinct founder queens, which appear to have originated from the same neighboring monogyne population. Multiple asexual/polygyne genomes are transmitted undiluted in this system, but sterile workers produced with sperm from a sexually-reproducing/monogyne population are necessary for the persistence of these lineages. The intersection of social polymorphism, facultative asexuality, and genetic caste determination marks this population of S. geminata as an embodiment of the diversity of ant reproductive systems and suggests previously unknown connections between these phenomena.
•Multi-queen colonies of a fire ant produce queens asexually but workers sexually•Single-queen colonies produce both queens and workers sexually•Queens in multi-queen colonies require sperm from single-queen colony males to produce workers•Distinct asexual/multi-queen lineages may stem from a sexual/single-queen population
Lacy et al. describe a socially polymorphic population of an ant in which multi-queen colonies produce queens asexually but produce workers sexually via matings with males from the sexually-reproducing single-queen social form. Two distinct asexual lineages from multi-queen colonies likely originated from the same sexual single-queen population.