Sperm Parasitism in Ants: Selection for Interspecific Mating and Hybridization

Abstract

Interspecific mating in eusocial Hymenoptera can be favored under certain conditions even if all hybrid offspring are completely infertile. This exploits two key features of the eusocial Hymenoptera: a haplodiploid genetic system and reproductive division of labor in females. Interspecifically mated queens can still produce viable sons that will mate intraspecifically. Apparent reduced fitness resulting from producing infertile daughter gynes can be also offset by advantages conferred by hybrid workers. An important advantage is likely to be superior ability at using marginal habitats. Interspecifically mated queens can nest in sites where intraspecific competition will be low. By mating interspecifically, a queen trades expected reproductive success through female offspring for a higher probability of achieving some reproductive success. Females that mate interspecifically can be considered "sperm parasites" on the males of the other species. I provide evidence that sperm parasitism is responsible for widespread hybridization in North America among two species of the ant subgenus Acanthomyops (genus Lasius), and review evidence for sperm parasitism in other hybridization phenomena in ants. Sperm parasitism in ants represents a novel form of social parasitism in ants and a dispersal polymorphism. It may also act as a precursor to the evolution of some other recently discovered phenomena, such as genetic caste determination.

Low genetic diversity in Polish populations of sibling ant species: Lasius niger (L.) and Lasius platythorax Seifert (Hymenoptera, Formicidae)

“…The recent morphological and genetic data revealed the surprising commonness of hybridization in ants (Feldhaar et al, 2008;Seifert, 2009), also among members of the genus Lasius (Pearson, 1983;Seifert, 1999;Umphrey, 2006). It seems plausible that in case of recently diverged species, as L. niger and L. platythorax, the reproductive barriers cannot completely prevent the possibility of interspecific hybridization.…”

Lifelong commitment to the wrong partner: hybridization in ants

“…richteri (Ross & Robertson 1990) showed increased levels of fluctuating asymmetry, and hybrid female sexuals of Temnothorax were smaller and less successful during colony foundation (Pusch et al 2006a) or had less ovarioles than those of the parental species (Plateaux 1979). Hybrid sterility or a generally lowered fitness of hybrid females might explain why hybrid female sexuals are rarely found despite the common occurrence of F 1 hybrid workers (Helms Cahan & Vinson 2003;Umphrey 2006).…”

“…Schrempf et al 2005). Female sexuals may therefore be less fastidious concerning the species of their mates than males and readily engage in what has been called sperm theft (or cleptogamy in Seifert 1999) or 'sperm parasitism' ( Umphrey 2006). By contrast, males should be strongly selected to efficiently discriminate against allospecific female sexuals and to avoid cross-species copulations.…”

Segregation distortion causes large-scale differences between male and female genomes in hybrid ants

“…Only a small percentage of the individuals within a nest reproduce whereas others, the workers, take care of a range of tasks and do not usually produce any offspring. Because of this, sterility of hybrid workers would have no or a minimal fitness cost on the colony level (13). In fact, hybridization may even be an advantage in social insects provided that the workers show hybrid vigor.…”

“…In haplodiploid Hymenoptera, males arise from unfertilized eggs and are haploid whereas females, both queens and workers, are diploid and produced biparentally. Allospecific mating is thus not necessarily an evolutionary dead end for a queen, because she can still produce nonhybrid males by laying unfertilized eggs (13). Even though F1 hybrid workers commonly occur in ants (14), there are few or no records on fertile hybrid queens or males (15).…”