Hybridization enables the fixation of selfish queen genotypes in eusocial colonies

Abstract

A eusocial colony typically consists of two main castes: queens that reproduce and sterile workers that help them. This division of labor, however, is vulnerable to genetic elements that favor the development of their carriers into queens. Several factors, such as intracolonial relatedness, can modulate the spread of such caste-biasing genotypes. Here we investigate the effects of a notable yet understudied ecological setting: where larvae produced by hybridization develop into sterile workers. Using mathematical modeling, we show that the coevolution of hybridization with caste determination readily triggers an evolutionary arms race between nonhybrid larvae that increasingly develop into queens, and queens that increasingly hybridize to produce workers. Even where hybridization reduces worker function and colony fitness, this race can lead to the loss of developmental plasticity and to genetically hard-wired caste determination. Overall, our results may help understand the repeated evolution toward remarkable reproductive systems (e.g., social hybridogenesis) observed in several ant species.

Chromosome-level genome assembly and annotation of two lineages of the ant Cataglyphis hispanica: stepping stones towards genomic studies of hybridogenesis and thermal adaptation in desert ants

“…The interdependent nature of the lineages could stem from a small number of recessive mutations biasing development toward the queen caste in each lineage. Such "royal cheats" (Hughes and Boomsma 2008) seem common in eusocial Hymenoptera and have been hypothesized to be at the origin of caste determination and possibly social hybridogenesis (Anderson et al 2008;Weyna et al 2021;Withrow and Tarpy 2018). In line with their observed phenotypic similarity, assemblies of the two lineages appear highly similar and colinear (Figure S3).…”

Ruling the unruly: Innovation in ant larval feeding led to increased caste dimorphism and social complexity

“…Strong dimorphism in species without passive larval morphology can also be achieved through more rare methods of larval caste fate regulation. Some species have caste fate partially or fully determined by genetic factors, biasing diploid larval totipotency (Anderson et al 2008, Weyna et al 2021. In some ant taxa, adults mildly injure their larvae and feed on their hemolymph.…”

“…Female embryos of social Hymenoptera are generally totipotent and can turn into either queens or workers. While caste fate is specified as early as in the egg in a few species (Anderson et al 2008, Weyna et al 2021, Qiu et al 2022, Schultner et al 2023, the prevailing belief is that 'environmental' (social) caste determination occurs during larval development for most species (Anderson et al 2008, Schwander et al 2010. In holometabolous insects, building size-differentiated castes relies on a non-homogenous distribution of larval feeding (Mirth and Riddiford 2007).…”

Toward greater realism in inclusive fitness models: the case of caste fate conflict in insect societies

“…Nevertheless, this was also unsatisfactory, as ideally one would be able to explain what cost function would be expected a priori, based on a detailed dynamic, microscopic model of how colonies grow and reproduce. The use of abstracted cost/benefit functions that are not mechanistically motivated is also common in other social evolution models (e.g., Dobata, 2012 ; Lehmann et al, 2008 ; Olejarz et al, 2015 ; Reuter & Keller, 2001 ; Weyna et al, 2021 ) and is in fact a recognized weakness and common criticism of many published inclusive fitness models ( Frank, 1998 ; Nowak et al, 2010 ). More broadly, in ecology and evolution in general, it is common for models to be formulated at a purely phenomenological level, and the implied assumptions that are made at a mechanistic level are not always clear (e.g., Brännström & Sumpter, 2005 ; Stefan et al, 2012 ).…”