Geographic patterns in colonial reproductive strategy inMyrmecina nipponica: Links between biogeography and a key polymorphism in ants

Abstract

The ability to express different phenotypes can help define species distributions by allowing access to, and exploitation of, new environments. Social insects employ two markedly different reproductive strategies with contrasting cost/benefit characteristics: independent colony foundation (ICF), which is associated with high dispersal range and high risk, and dependent colony foundation (DCF), characterized by low risk but low dispersal. The ant Myrmecina nipponica employs both of these strategies, with the frequency of each apparently varying between populations. We combine molecular data with data on reproductive strategy from different populations of this species throughout Japan to explore how this polymorphism is linked to environmental factors and whether this relationship can help explain the current and historical biogeography of this species. Reproductive strategy exhibited a strong geographic pattern, with ICF predominant in southern populations and DCF more common in northern and southern highland populations. Molecular analyses clearly divided populations into broad geographic regions, with the southern lowland populations basal to (southern highland (+ northern)) populations. Intra‐population polymorphism in colony‐founding strategy was widespread, and polymorphism was reconstructed as the likely ancestral state. The frequency of different strategies was linked with climate, with DCF more common in colder areas. A recent inferred origin to the northern lineage suggests that colonization of northern Japan was a rapid event coincident with warming at the end of the Last Glacial Maxima, likely facilitated by the cold‐adaptive advantages of DCF. We discuss how such polymorphisms could help explain the biogeography of this and other social insects.

Cooperation by ant queens during colony-founding perpetuates alternative forms of social organization

“…In social insects, as in other group-living animals, social organization has long been considered a phenotypically plastic trait (Stacey and Bock 1978 ; Koenig et al 1992 ; Wcislo 1997 ; Heinze 2008 ; Gadau et al 2009 ; Maher and Burger 2011 ; Schradin et al 2012 ). This is because key social traits, like mode of colony-founding, levels of cooperation, and number of reproductive queens within colonies, vary with colony development and/or with ecological variables in many species (Ross and Keller 1995 ; Wcislo 1997 ; Herbers and Banschbach 1999 ; Cronin 2001 ; Ingram 2002 ; Heinze 2008 ; Field et al 2010 ; Trettin et al 2014 ; Cronin et al 2020 ). Specifically in ants, colonies founded by a single queen can adopt additional queens as they grow (Bourke and Franks 1995 ), and colonies founded by multiple queens often retain only one queen after the first cohort of workers emerges (Bernasconi and Strassmann 1999 ).…”

Habitat fragmentation selects for low dispersal in an ant species

“…The relative abundance of each strategy varies with environmental factors, i.e. altitude in M. nipponica [17], habitat patchiness and isolation in L. canadensis [16] and drought in Chelaner sp. [15].…”

To disperse or compete? Coevolution of traits leads to a limited number of reproductive strategies

“…For instance, the plant Crepis sancta can produce small wind dispersed seeds that have low competitiveness, or larger seeds that disperse shorter distance but are more competitive because they germinate earlier (Cheptou et al 2008), and in the case of marine invertebrates, planktotrophic taxa (suffering from high mortality) tend to be smaller and disperse further than lecithotrophic taxa (Rundle et al 2009, more examples in Material and methods). In many of these organisms, reproductive investment and offspring size are relatively unconstrained, which results in a large variability of reproductive strategies (Heinze 1993, Cronin et al 2020). In plants, for example, seed size and investment range over several orders of magnitude (Eriksson 2008), and in social insects, new colonies can be started by individual queens or swarms of thousands of workers and queens (Cronin et al 2013).…”