When every sperm is sacred: the emergence and decline of superorganismal chimeras

Those with even a passing interest in natural history have likely noticed the nuptial flights of ants. Be it on windless summer afternoons in temperate cities or upon the arrival of the first rains in the seasonal tropics, the synchronous mass emergence of winged ants over large areas is spectacular. However, these events are also ephemeral – you may easily miss them unless you are in the right place at the right time. Patient observers will be rewarded by seeing countless queens landing and shedding their wings to start searching for a place to dig their nest. These lucky survivors were inseminated by one or several males high up in the air while avoiding assaults from predatory birds. They are now ready to initiate a new colony of sterile workers whose cohorts need to increase in numbers for several years before the ensuing superorganism (Wheeler 1911) can produce winged reproductives that will start a next generation. A newly inseminated ant queen is analogous to a helicopter seed of a maple tree that is carried away by the wind to a distant place where it will produce a new tree or perish. The seed was fertilized by an airborne pollen while still on the tree, while the ant queen was inseminated during dispersal, but this difference does not matter functionally. Neither the maple seed nor the ant queen will ever be fertilized again later in life. The maple zygote will become a germinating embryo, using its endosperm reserves to grow roots and photosynthesizing leaves to become a mature organism; the ant queen will metabolize her now superfluous wing muscles to release proteins for producing eggs, use her stored sperm to fertilize them, and break down her fat reserves to survive until the first workers hatch and start bringing in food. Both the maple tree and the ant colony will need to grow for a number of years before they can reproduce and both may continue to reproduce for many years to come. Ant colonies are families and maple trees clones, but their deep (super)organismal history offers further intriguing analogies. Foundation by a single zygote consisting of two lifetime-committed gametes was a necessary condition for the first emergence of complex animal and plant organismality (Fisher, Cornwallis & West 2013), similar to strict lifetime monogamy having been a necessary condition for the evolutionary origins of eusocial superorganismality (Hughes et al. 2008). However, some lineages of ants, bees and wasps secondarily evolved to have genetically chimeric colonies that result from queens being inseminated by multiple males on the same nuptial flight (Boomsma & Ratnieks 1996). Chimeric superorganismality has no analogy in multicellular organisms because polyspermy – the simultaneous fertilization of an egg by more than one sperm – makes zygotes inviable (Hemmings & Birkhead 2015). Long-lived chimeric superorganismality emerged in the honeybees, the fungus-growing ants, the seed harvester ants and the army ants where all queens have stored sperm from 2 to more than 20 males, resulting in colonies consisting mostly of half-siblings (Boomsma, Kronauer & Pedersen 2009). In a new study, Aron et al. (2015) now add Cataglyphis desert ants to the rather short list of social insect genera where populations always have colonies with multiply inseminated queens. This new study by Aron et al. (2015) is remarkable because it shows that chimeric superorganismality, although evolutionarily derived for ants in general, was ancestral in the genus Cataglyphis and has become secondarily reversed to varying degrees. No species ever returned to exclusive single insemination, but four of the 15 species investigated had some colonies and another four species had most colonies founded by a once-mated queen. Ant lineages with obligate multiple insemination of queens normally have mature colony sizes of at least ten thousand and up to several millions, so these partial reversals may be related to desert ants having at most a few thousand workers per colony. More importantly, however, these reversals offered an unusual opportunity to explore how sperm competition affects male traits related to reproductive investment. As the authors show, the number of sperm produced by Cataglyphis males became reduced in proportion to the risk of sperm competition, but sperm length and male body size were not affected. Decreasing investment in sperm lottery tickets when the odds improve is intriguing because ant sperm competition is restricted to the few hours that ejaculates coexist in the bursa copulatrix of queens. In this phase, queens receive more sperm than they can store, so it is in their interest to allow sperm competition when it ensures they end up storing the fittest fraction to fertilize eggs for the rest of their lives. However, this perspective changes dramatically after *Correspondence author. E-mail: jjboomsma@bio.ku.dk