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Fecundity Determines the Outcome of Founding Queen bioRxiv preprint doi: https://doi.org/10.1101/2020.11.20.391359; this version posted November 21, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 2 3 4 5 6 7 8 9 10 Fecundity determines the outcome of 11 founding queen associations in ants 12 13 Eva-Maria Teggers1, Falk Deegener1, Romain Libbrecht1 14 1Institute of Organismic and Molecular Evolution, Johannes Gutenberg University of Mainz, Germany 15 16 17 18 19 Short title 20 Benefits and factors of pleometrosis 21 22 Correspondence 23 Romain Libbrecht 24 Hanns-Dieter-Hüsch-Weg 15 25 55128 Mainz - Germany 26 [email protected] 27 +49 6131 3927852 28 bioRxiv preprint doi: https://doi.org/10.1101/2020.11.20.391359; this version posted November 21, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 29 Abstract 30 Animal cooperation evolved because of its benefits to the cooperators. Pleometrosis in ants - the 31 cooperation of queens to found a colony - benefits colony growth, but also incurs costs for some of the 32 cooperators because only one queen usually survives the association. While several traits are associated 33 with queen survival, they tend to be confounded and it is unclear which factor specifically determines 34 the outcome of pleometrosis. In this study, we used the ant Lasius niger to monitor offspring production 35 in colonies founded by one or two queens. Then, we experimentally paired queens that differed in 36 fecundity but not in size, and vice versa, to disentangle the effect of these factors on queen survival. 37 Finally, we investigated how fecundity and size differed between queens depending on whether they 38 were chosen as pleometrotic partners. Our results indicate that pleometrosis increased and accelerated 39 worker production via a nutritional boost to the larvae. The most fecund queens more frequently 40 survived the associations, even when controlling for size and worker parentage, and queens selected as 41 pleometrotic partners were less fecund. Our results are consistent with fecundity being central to the 42 onset and outcome of pleometrosis, a typical case of cooperation among unrelated animals. 43 44 Keywords 45 Pleometrosis; Social insects; Cooperation 46 bioRxiv preprint doi: https://doi.org/10.1101/2020.11.20.391359; this version posted November 21, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 47 Introduction 48 While animal cooperation typically occurs among related individuals (Hamilton, 1964), there are cases 49 of unrelated cooperators in some mammal, bird and insect species (Bernasconi & Strassmann, 1999). 50 These have raised interesting questions on the origin, maintenance and benefits of cooperation among 51 unrelated animals. Such questions include how the internal (e.g., physiology) and external (e.g., 52 environment) conditions affect the decision to behave cooperatively, the benefits of cooperation, and its 53 outcome. While social insects are typical model systems for kin-based cooperation, the early stage of 54 the colony life of some ant species provides a classic example of cooperation among unrelated partners 55 (Bernasconi & Strassmann, 1999). 56 Pleometrosis in ants is the foundation of colonies by two or more cooperating newly-mated queens that 57 settle in the same nest site after a nuptial flight (Bartz & Hölldobler, 1982; Hölldobler & Wilson, 1977; 58 Sommer & Hölldobler, 1995; Wheeler, 1917). In some cases, pleometrosis results in mature multiple- 59 queen colonies, as in pleometrotic populations of harvester ants (Johnson, 2004; Overson et al., 2016). 60 However, in most species, pleometrotic associations are only transitory: the queens stay together to 61 produce eggs, but upon worker emergence, queens engage in fights (sometimes initiated and/or joined 62 by the workers) until a single queen survives (Bartz & Hölldobler, 1982). Pleometrosis results in an 63 earlier production of larger groups of workers compared to solitary foundation, which may be beneficial 64 in dense populations where young colonies compete for food and brood raiding can be common 65 (Deslippe & Savolainen, 1995; Johnson, 2004; Madsen & Offenberg, 2017; Rissing & Pollock, 1987; 66 Sommer & Hölldobler, 1995; Trunzer et al., 1998). How pleometrosis benefits colony growth remains 67 unclear (Brütsch et al., 2017; Pull et al., 2013). 68 The queens that do not survive the pleometrotic associations have no fitness benefits, as they die before 69 producing sexuals (the fertile individuals that are only produced in mature colonies). Thus, 70 understanding the factors that determine which queens survive the associations would allow researchers 71 to draw and test hypotheses on whether or not queens with given characteristics should decide to 72 cooperate with other queens, as well as understand previous reports of such queen decisions (Nonacs, 73 1992; Sommer & Hölldobler, 1995). bioRxiv preprint doi: https://doi.org/10.1101/2020.11.20.391359; this version posted November 21, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 74 Several determinants of queen survival have been identified. Winning queens tend to be larger (Aron et 75 al., 2009; Bernasconi & Keller, 1996; Bernasconi & Keller, 1998; Nonacs, 1990), heavier (Nonacs, 76 1990, 1992; but see Sommer & Hölldobler, 1995), to spend more time on the brood pile (Balas & Adams, 77 1996; Holman et al., 2010), and to lose less weight during colony foundation (Balas & Adams, 1996; 78 Bernasconi & Keller, 1996). However, these reports may have been subject to confounding effects 79 because the factors tested are usually interconnected. For example, size and mass may correlate with 80 fecundity (Aron et al., 2009), which in turn influences worker production and therefore worker parentage 81 in the offspring. One strategy to control for such confounded factors is to experimentally pair queens 82 that differ in one factor but not in others, thus allowing the identification of factors that affect queen 83 survival irrespective of others. 84 In this study, we used the black garden ant Lasius niger to study cooperation among unrelated 85 individuals in pleometrotic associations. We first quantified the benefits of pleometrosis in terms of 86 brood production and development. Then we tested whether fecundity and size, two factors that may be 87 associated with queen survival (Aron et al., 2009; Balas & Adams, 1996; Bernasconi & Keller, 1996; 88 Nonacs, 1990) were correlated. We investigated the effect of fecundity and size on queen survival in 89 experimental pleometrotic associations that differ in one factor but not the other, while controlling for 90 worker parentage. Finally, we compared fecundity and size between queens that were selected as 91 pleometrotic partners and queens that were not. 92 bioRxiv preprint doi: https://doi.org/10.1101/2020.11.20.391359; this version posted November 21, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 93 Methods 94 Sample collection 95 We used L. niger as study organism because queens in this species commonly found new colonies in 96 pleometrotic associations that consist of typically unrelated individuals (Sommer & Hölldobler, 1995). 97 We collected 276 L. niger founding queens in Mainz, Germany right after nuptial flights on June 26th 98 2017 (cohort 1, 138 queens), July 9th 2017 (cohort 2, 138 queens) and July 4th 2020 (cohort 3, 135 99 queens). The queens were housed in glass test tubes (10*1.2cm) with water blocked by a cotton ball, 100 and then kept in the dark at 21°C. 101 Experimental designs 102 We randomly selected 45 queens from cohort 2 to investigate the benefits of pleometrosis. Half the test 103 tubes contained a single queen (n = 15), and the other half contained two queens (n = 15). Then we 104 recorded the number of eggs, larvae, pupae and workers three times a week for 53 days. Upon emergence 105 of the first workers, we placed the tubes in larger plastic boxes (11*15*3cm) and fed the colonies once 106 a week with a mixture of honey, eggs, agar and water (Bhatkar & Whitcomb, 1970). Eight queens died 107 over the course of the experiment: Three queens in the treatment with one queen died 4, 11 and 16 days 108 after set-up, and were removed from the analyses. Five queens in the treatment with two queens died 109 37, 42 (2) and 49 (2) days after set-up. In each of those five cases, one queen of the two queens survived. 110 These tubes were kept in the analyses because queen execution is expected in pleometrotic associations. 111 We used 231 queens (138 from cohort 1, 93 from cohort 2) to investigate the effect of size and fecundity 112 on queen survival. On day 17 after the nuptial flights, we recorded the number of brood items (eggs and 113 larvae) in each tube, and used this measure as a proxy for fecundity, thus assuming that egg production 114 changes similarly over time across queens.
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