Substantial direct fitness gains of workers in a highly eusocial ant

Abstract

Hamilton's theory of inclusive fitness suggests that helpers in animal societies gain fitness indirectly by increasing the reproductive performance of a related beneficiary. Helpers in cooperatively breeding birds, mammals and primitively eusocial wasps may additionally obtain direct fitness through inheriting the nest or mating partner of the former reproductive. Here, we show that also workers of a highly eusocial ant may achieve considerable direct fitness by producing males in both queenless and queenright colonies. We investigated the reproductive success of workers of the ant Temnothorax crassispinus in nature and the laboratory by dissecting workers and determining the origin of males by microsatellite analysis. We show that workers are capable of activating their ovaries and successfully producing their sons independently of the presence of a queen. Genotypes revealed that at least one fifth of the males in natural queenright colonies were not offspring of the queen. Most worker-produced males could be assigned to workers that were unrelated to the queen, suggesting egg-laying by drifting workers.

Queen execution in a monogynous ant

“…Colonies of Temnothorax crassispinus (Karavajev 1926) consist of only a few dozens or hundreds of workers and a single, singly mated queen. Colony structure is relatively fluid, as colonies may seasonally split and merge, adopt alien workers or are usurped by alien queens (Giehr, Wallner, et al., 2020). Nests are found in acorns and rotting twigs in deciduous forests throughout Eastern Central and Eastern Europe (Mitrus, 2015; Seifert, 2018; Strätz & Heinze, 2004; Tichá & Štys, 2002).…”

“…In total, we collected 436 colonies around Regensburg, Germany. Data about male paternity and genetic structure of these colonies are analyzed in a separate manuscript, in which also details about collecting and colony maintenance are given (Giehr, Wallner, et al., 2020). In short, individual colonies were transferred from their natural nests into separate plastic boxes (10 × 10 × 3 cm 3 ) with a plaster floor and a Plexiglas ® frame sandwiched between two microscope slides serving as nest.…”

“…Colonies were fed with pieces of cockroaches and honey twice per week in spring and summer, once per week at day temperatures below 15°C, and once every two weeks at day temperatures below 5°C. Nests were protected with fleece at temperatures below 0°C (see also Giehr, Wallner, et al., 2020).…”

“…Details on microsatellite analyses are given in Giehr, Wallner, et al. (2020). In short, we extracted DNA using the CTAB method (modified from Sambrook and Russell (2001) and amplified six DNA at six microsatellite loci by PCR (GT218, Hamaguchi et al., 1993; 2MS17, Suefuji et al., 2011; L5, Foitzik et al., 1997; L18, Foitzik et al., 1997; Ant3993, Butler et al., 2014, GT1 (Bourke et al., 1997).…”

“…We examined worker reproductive success over several years in originally queenright colonies and colonies, in which workers had actively expelled and/or killed their queen (“orphaned colonies”). Queens of monogynous Temnothorax have been observed to have a mean survival time in the laboratory of 5.9–15 years (Keller, 1998; Plateaux, 1971), but previous studies indicated a high queen turn over and frequent colony usurpations and fusions in T. nylanderi (Foitzik & Heinze, 1998, 2000) and its sibling species T. crassispinus (Giehr et al., 2020; Giehr, Wallner, et al., 2020; Strätz & Heinze, 2004).…”