The ecological benefits of larger colony size may promote polygyny in ants

Abstract

How polygyny evolved in social insect societies is a long-standing question. This phenomenon, which is functionally similar to communal breeding in vertebrates, occurs when several queens come together in the same nest to lay eggs that are raised by workers. As a consequence, polygyny drastically reduces genetic relatedness among nestmates. It has been suggested that the short-term benefits procured by group living may outweigh the costs of sharing the same nesting site and thus contribute to organisms rearing unrelated individuals. However, tests of this hypothesis are still limited. To examine the evolutionary emergence of polygyny, we reviewed the literature to build a data set containing life-history traits for 149 Palearctic ant species and combined this data set with a reconstructed phylogeny. We show that monogyny is the ancestral state and that polygyny has evolved secondarily and independently throughout the phylogenetic tree. The occurrence of polygyny is significantly correlated with larger colony size, dependent colony founding and ecological dominance. Although polydomy (when a colony simultaneously uses several connected nests) tends to occur more frequently in polygynous species, this trend is not significant when phylogenetic history is accounted for. Overall, our results indicate that polygyny may have evolved in ants in spite of the reduction in nestmate relatedness because large colony size provides immediate ecological advantages, such as the more efficient use of temporal food resources. We suggest that the competitive context of ant communities may have provided the conditions necessary for the evolution of polygyny in some clades.

An Organismal Perspective on the Evolution of Insect Societies

“…However, the sizes of queens seem evolutionarily highly flexible. Decreases in queens size have occurred especially in multiple queen colonies that have lost independent colony founding, and queen number may vary even within species (Rüppell et al, 1998;Heinze and Keller, 2000;Sundström et al, 2005;Steiner et al, 2006;Boulay et al, 2014).…”

“…Young queens mate locally and are recruited back to their natal colonies. Such life histories have evolved repeatedly in ants, and are phylogenetically very flexible (Sundström et al, 2005;Cronin et al, 2013;Boulay et al, 2014), but are absent or rare in other social Hymenoptera and termites (Boomsma et al, 2014). Secondary polygyny is often associated with large colony size (Rosengren et al, 1993;Boulay et al, 2014), suggesting an opposite pattern to marine invertebrates.…”

“…Such life histories have evolved repeatedly in ants, and are phylogenetically very flexible (Sundström et al, 2005;Cronin et al, 2013;Boulay et al, 2014), but are absent or rare in other social Hymenoptera and termites (Boomsma et al, 2014). Secondary polygyny is often associated with large colony size (Rosengren et al, 1993;Boulay et al, 2014), suggesting an opposite pattern to marine invertebrates. In contrast, a correlation between large offspring size and sperm casting is possible, similarly to marine invertebrates: many polygynous systems have life cycles (Debout et al, 2007), where new colonies are founded through large propagules containing both queens and workers (see below), which constitutes large offspring size at the superorganism level.…”

Inbreeding tolerance as a pre‐adapted trait for invasion success in the invasive ant Brachyponera chinensis

“…This may lead to a loss of nestmate recognition and a collapse of colony boundaries (Giraud, Pedersen, & Keller, ; Suarez et al., ), supporting the development of supercolonies: widespread colonies formed of several interconnected nests containing several, up to thousands of queens (Helanterä, Strassmann, Carrillo, & Queller, ; Holway, Lach, Suarez, Tsutsui, & Case, ; Suarez et al., ). This social organization provides colonies rapid growth, a higher probability of survival and an earlier onset of the reproduction stage (Boomsma, Huszár, & Pedersen, ; Boulay, Arnan, Cerdá, & Retana, ). Ultimately, unicoloniality provides a strong ecological advantage and raises the likelihood of invasion by allowing such colonies to reach high worker densities and lower intraspecific competition, resulting in interspecific dominance (Holway & Suarez, ; Le Breton, Jourdan, Chazeau, Orivel, & Dejean, ).…”

Life-history evolution in ants: the case ofCardiocondyla

“…In social Hymenoptera, polygyny is thought to be a derived trait [40] that evolved whenever environmental conditions promoted large colony size [32] or facilitated colony propagation by fragmentation of the natal colony and the dispersal of groups of workers and queens ('budding' e.g. [33,38,39]).…”