Sperm competition increases sperm production and quality inCataglyphisdesert ants

Abstract

Sperm competition is a pervasive evolutionary force that shapes sperm traits to maximize fertilization success. Indeed, it has been shown to increase sperm production in both vertebrates and invertebrates. However, sperm production is energetically costly, which may result in trade-offs among sperm traits. In eusocial hymenopterans, such as ants, mating dynamics impose unique selective pressures on ejaculate. Males are sperm limited: they enter adulthood with a fixed amount of sperm that will not be renewed. We explored whether sperm competition intensity was associated with sperm quantity and quality (i.e. sperm viability and DNA fragmentation) in nine Cataglyphis desert ants. Our results provide phylogenetically robust evidence that sperm competition is positively correlated with sperm production and sperm viability. However, it was unrelated to sperm DNA integrity, indicating the absence of a trade-off involving this trait. These findings underscore that sperm competition may strongly mould sperm traits and drive reproductive performance in eusocial Hymenoptera.

Accessory gland size increases with sperm competition intensity in Cataglyphis desert ants

“…In Cataglyphis, AG size and sperm production are positively associated with sperm competition intensity which suggests that seminal fluid boosts sperm function (Ramm, 2020). In the same vein, it has been shown that sperm competition selects for increased sperm quality in Cataglyphis: in species with highly polyandrous females, males produce more viable sperm with lower levels of DNA fragmentation (Degueldre and Aron, 2023). Seminal fluid could help maintain high levels of sperm quantity and quality by furnishing (i) antioxidant enzymes that limit oxidative stress (Weirich et al, 2002;Collins et al, 2006;Baer et al, 2009); (ii) substances that sustain sperm metabolism (Blum et al, 1962;Alumot et al, 1969); and (iii) antimicrobial and antifungal enzymes (Baer et al, 2009;Peng et al, 2015;Cheŕasse et al, 2018;Davila et al, 2018).…”

“…Sperm production data for the nine study species were obtained from Degueldre and Aron (2023). Briefly, both accessory testes from each male were dissected in semen diluent.…”

“…For each species, sperm competition intensity was inferred from paternity frequency (i.e., the number of males that father the offspring of a queen; Aron et al, 2016;Degueldre and Aron, 2023). Data on paternity frequency were obtained from previous studies in which microsatellite loci were used to determine patriline number.…”

“…Third, polyandry has evolved repeatedly in ants, bees, and wasps (Hughes et al, 2008), creating conditions conducive to sperm competition in multiple species. In the few studies looking at how sperm competition influences sperm traits, it has been observed that sperm competition may select for (i) enhanced sperm production (ants: Baer and Boomsma, 2004;Aron et al, 2016;Degueldre and Aron, 2023), (ii) increased sperm size (bumble bees: Baer et al, 2003). Furthermore, seminal fluid can promote male fitness by (i) enhancing sperm viability (honey bees: den Boer et al, 2009); (ii) incapacitating rival sperm when females have multiple mates (ants and honey bees: den Boer et al, 2010); and (iii) reducing female promiscuity by either generating a mating plug (ants: Baer, 2011; bumble bees: Duvoisin et al, 1999;Brown et al, 2002) or by negatively affecting the eyesight of females during the mating flight (honey bees: Liberti et al, 2019).…”

“…Desert ants of the genus Cataglyphis are well suited to explore the association between seminal fluid production and sperm production. Indeed, (i) the degree of polyandry varies almost 10fold across species (range of the mean number of male mates: 1.07 -8.5; Aron et al, 2016) and (ii) sperm production increases with sperm competition intensity (Aron et al, 2016;Degueldre and Aron, 2023). Using phylogenetically controlled analyses, we explored the relationship, and potential trade-off, between accessory gland size-a proxy for seminal fluid production-and sperm production in nine species of Cataglyphis ants experiencing various degrees of sperm competition.…”