Sperm production characteristics vary with level of sperm competition in Cataglyphis desert ants

Abstract

1. Under polyandry, males are selected to produce more competitive ejaculates. Theoretical models have explored how the mechanism of sperm competition drives males to partition investment within an ejaculate between sperm quantity and quality. The raffle-based competition model predicts that increased level of sperm competition selects for larger numbers of sperm in ejaculates. Sperm competition is also thought to promote the evolution of longer sperm, because longer sperm could be faster. 2. In eusocial Hymenoptera, the mating system imposes unique selective pressures on male ejaculates. Males are short lived; they reach adulthood with a finite amount of spermatozoa, and they mate typically with a single or a few females and die. The actual number of spermatozoa stored in their accessory testes at emergence is thus a reliable measure of total investment into sperm production. In a comparative study of 15 species of Cataglyphis desert ants, we used phylogenetically controlled analyses to investigate relationships between levels of sperm competition, sperm production and sperm length. We measured sperm production by quantifying the number of spermatozoa present in testes, instead of using a proxy measure such as size of testes. Multiple queen mating is the ancestral state in the genus but reduction in mating frequency evolved secondarily and independently in some clades, providing a unique opportunity to examine how reduction from multiple to single mating influences sperm traits. 3. Our results provide phylogenetically robust evidence that species experiencing greater levels of sperm competition produce more sperm. After controlling for male size, investment in sperm production decreases significantly according to the sequence obligatory multiple queen mating > multiple-single queen mating > single-double queen mating. Furthermore, the number of spermatozoa produced per male decreases significantly with reduction in paternity frequency for each species. In contrast, neither sperm length nor male size was significantly associated with the mating system classes or the number of patrilines. 4. Our measures of sperm number provide the first direct evidence that sperm production covaries with the level of sperm competition in a eusocial insect. Given the reversal from multiple to single mating in Cataglyphis, our comparative analysis also shows convincingly that reduction in sperm competition influences sperm traits.

From storage to delivery: sperm volume and number of spermatozoa inside storage organs and ejaculates in males ofTimogenes elegans(Scorpiones: Bothriuridae)

“…Bukowski & Christenson (1997) also showed that sperm stored inside the female's spermatheca were on the order of 1 3 10 4 . However, sperm counts in scorpions more closely resembled ejaculates of other arthropods (e.g., Brown & Knouse 1973;Swallow & Wilkinson 2002;Sato et al 2006;Vahed 2006;Dallai et al 2009;Aron et al 2016). Similar to what happened with scorpions' seminal vesicles, Snow & Andrade (2004) also reported a correlation between the number of spermatozoa in the right and left pedipalps.…”

Cytonuclear incongruences hamper species delimitation in the socially polymorphic desert ants of the Cataglyphis albicans group in Israel

“…Multiple mating per queen could also have been selected to improve post‐copulatory sperm competition (Parker, ; Simmons, ). In Cataglyphis species, paternity frequency drives the evolution of male investment in sperm production, as males from highly polyandrous species tend to produce more and longer spermatozoa than males from weakly polyandrous species (Aron et al ., ). To date, reversion to single mating has been reported only twice in this genus, in the C. altisquamis and C. emmae groups (Leniaud et al ., ; Amor & Ortega, ; Aron et al ., ).…”

When every sperm is sacred: the emergence and decline of superorganismal chimeras

“…In a new study, Aron et al . () now add Cataglyphis desert ants to the rather short list of social insect genera where populations always have colonies with multiply inseminated queens.…”

“…This new study by Aron et al . () is remarkable because it shows that chimeric superorganismality, although evolutionarily derived for ants in general, was ancestral in the genus Cataglyphis and has become secondarily reversed to varying degrees. No species ever returned to exclusive single insemination, but four of the 15 species investigated had some colonies and another four species had most colonies founded by a once‐mated queen.…”

“…Long-lived chimeric superorganismality emerged in the honeybees, the fungus-growing ants, the seed harvester ants and the army ants where all queens have stored sperm from 2 to more than 20 males, resulting in colonies consisting mostly of half-siblings (Boomsma, Kronauer & Pedersen 2009). In a new study, Aron et al (2015) now add Cataglyphis desert ants to the rather short list of social insect genera where populations always have colonies with multiply inseminated queens.…”