Everything About Ant Reproductive Biology is Bizarre

Sam Gregory wrote this post as a project for Dr. Stacy Krueger-Hadfield’s Scientific Communication course at the University of Alabama at Birmingham. Sam earned a BS in biology and BFA in studio art from Birmingham-Southern College, and is currently pursuing an MS in Biology at UAB. He is fascinated by Alabama’s diverse ecosystems, particularly the currently-threatened arthropod communities that serve a foundational role in these systems.

In a recent article, researchers evaluated reproductive systems within Cataglyphis, a genus of desert ants (Kuhn et al., 2020). Two unusual systems had been observed within the genus. To understand Cataglyphis reproduction, though, one must first understand conventional ant reproduction.

The vast majority of ants in a colony are workers. They are female, but infertile. Workers grow from the eggs of the colony’s queen (Wheeler, 2016). A few eggs develop into winged alates – either queens, which are fertile females, or males, which are haploid and hatch from unfertilized eggs (White, 1984). Every year, alates fly from the colony en massein search of mates (Wilson, 1957). Males die soon after mating, and queens maintain the sperm in a specialized organ (Wheeler & Krutzch, 1994), allowing them to fertilize eggs for the rest of their lives, potentially decades in some species (Keller, 1998). Each queen then finds a safe place to hide while her workers reach maturity. In many species, the queen raises her first offspring to adulthood without eating (Keller & Passera, 1989).

Diagram of the standard ant reproductive mode in Camponotus pennsylvanicus by Sam Gregory

This is far more than a string of fun facts. 

This paradigm allows non-reproductive individuals to shoulder risks while queens remain safe. This strategy is a major factor behind the evolutionary success of Formicidae, the family of ants, which comprise a remarkable portion of Earth’s land animal biomass (Wilson, 1985). This makes ants an interesting clade for examining the evolution of reproductive systems. Unusual reproduction creates unique selection pressures, leading subclades to adopt even stranger reproductive modes (Heinze & Tsuji, 1995).

Kuhn et al. (2020) were interested in two unusual reproductive systems seen in the genus Cataglyphis. In some species, queens produce workers sexually, but produce new queens by fertilizing their own eggs. This is called conditional use of sex. Their colonies are made robust by variation among workers, while reproductive offspring receive only the queen’s DNA (Pearcy et al., 2004).

Diagram of conditional use of sex in Cataglyphis cursor by Sam Gregory

Another group within Cataglyphis reproduces by a means termed clonal social hybridogenesis. These ants also use sex conditionally, but a “species” (though we are well past the point where species concepts break down) consists of two genetic lineages. The queens selectively mate with males of the opposite lineage to produce workers. These workers are diverse and robust, without the disadvantage to fertility that often comes with hybridization, as workers are sterile anyway (Burke & Arnold, 2001Umphrey, 2006).

To evaluate the evolutionary history of these reproductive modes, the researchers dug up Cataglyphis colonies across Europe and the Middle East. By genotyping reproducing queens, unmated queens, and workers, they ascertained each species’ reproductive strategy. Male haploidy provided a huge advantage, since the genotype of the colony’s long-dead father can be inferred from those of the workers and queen. They then investigated whether a species consisted of multiple genetic clusters, and if so, whether the clusters selectively interbred (Kuhn et al., 2020).

Figure 1. Principal Coordinates Analysis showing favored inter-lineage mating between distinct genetic clusters (single exception denoted by a red line) in C. cretica (Kuhn et al., 2019)

The researchers found numerous cases of both conditional sex and clonal social hybridogenesis. Interestingly, there was precisely one instance of intra-lineage mating in a “species” that normally undergoes hybridogenesis (Cataglyphiscretica) (Figure 1). This colony was abnormally small, potentially reflecting the intuitive advantage of inter-lineage mating (though a single case is far from definitive evidence) (Kuhn et al., 2019).

In the proposed phylogeny (Figure 2), each reproductive mode arose multiple times, and conditional use of sex appears to be a prerequisite to clonal social hybridogenesis (Kuhn et al., 2020).

Figure 2. A portion of the Cataglyphis phylogenetic tree constructed by Kuhn et al. (2019)

This study has shed further light on the broader topic of selection pressures relating to modes of reproduction. Some questions remain unanswered, though. The researchers note that every pair of hybridogenetic lineages appears to have diverged recently, despite the far less recent evolution of conditional sex (Kuhn et al., 2020). 

This could indicate that such systems arise commonly, but are unsustainable, as rising homozygosity destroys queen viability. Alternatively, these lineages may not be totally isolated, with some low level of gene flow occurring (Kuhn et al., 2020). In either case, further research into these systems would do a great deal to advance the understanding of reproductive evolution.

References

Burke, J. M., & Arnold, M. L. (2001). Genetics and the Fitness of Hybrids. Annual Review of Genetics35, 31–52.

Heinze, J., & Tsuji, K. (1995). Ant reproductive strategies. Researches on Population Ecology, Vol. 37, pp. 135–149.

Keller, L. (1998). Queen lifespan and colony characteristics in ants and termites. Insectes Sociaux45(3), 235–246.

Keller, Laurent, & Passera, L. (1989). Size and fat content of gynes in relation to the mode of colony founding in ants (Hymenoptera; Formicidae). Oecologia, 80(2), 236–240.

Kuhn, A., Darras, H., Paknia, O., & Aron, S. (2020). Repeated evolution of queen parthenogenesis and social hybridogenesis in Cataglyphis desert ants. Molecular Ecology, 29: 549-564.

Pearcy, M., Aron, S., Doums, C., & Keller, L. (2004). Conditional use of sex and parthenogenesis for worker and queen production in ants. Science,306(5702), 1780–1783.

Umphrey, G. J. (2006). Sperm parasitism in ants: Selection for interspecific mating and hybridization. Ecology87(9), 2148–2159.

Wheeler, D. E. (2016). The Developmental Basis of Worker Caste Polymorphism in Ants. The American Naturalist138(5), 1218–1238.

Wheeler, D. E., & Krutzsch, P. H. (1994). Ultrastructure of the spermatheca and its associated gland in the ant Crematogaster opuntiae (Hymenoptera, Formicidae). Zoomorphology114(4), 203–212.

White, M. J. D. (1984). Chromosomal mechanisms in animal reproduction. Bolletino Di Zoologia51(1–2), 1–23.

Wilson, E. O. (1957). The Organization of a Nuptial Flight of the Ant Pheidole Sttarches Wheeler. Psyche (New York)64(2), 46–50.

Wilson, Edward O. (1985). The Sociogenesis of Insect Colonies. Science228(4707), 1489–1495.

About Stacy Krueger-Hadfield

I am a marine evolutionary ecologist interested in the impacts of seascapes and complex life cycles on marine population dynamics. I use natural history, manipulative field experiments and population genetic and genomic approaches with algal and invertebrate models in temperate rocky shores,estuaries and the open ocean.
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