Sperm use economy of honeybee (Apis mellifera) queens

Abstract

The queens of eusocial ants, bees, and wasps only mate during a very brief period early in life to acquire and store a lifetime supply of sperm. As sperm cannot be replenished, queens have to be highly economic when using stored sperm to fertilize eggs, especially in species with large and long‐lived colonies. However, queen fertility has not been studied in detail, so that we have little understanding of how economic sperm use is in different species, and whether queens are able to influence their sperm use. This is surprising given that sperm use is a key factor of eusocial life, as it determines the fecundity and longevity of queens and therefore colony fitness. We quantified the number of sperm that honeybee (Apis mellifera) queens use to fertilize eggs. We examined sperm use in naturally mated queens of different ages and in queens artificially inseminated with different volumes of semen. We found that queens are remarkably efficient and only use a median of 2 sperm per egg fertilization, with decreasing sperm use in older queens. The number of sperm in storage was always a significant predictor for the number of sperm used per fertilization, indicating that queens use a constant ratio of spermathecal fluid relative to total spermathecal volume of 2.364 × 10−6 to fertilize eggs. This allowed us to calculate a lifetime fecundity for honeybee queens of around 1,500,000 fertilized eggs. Our data provide the first empirical evidence that honeybee queens do not manipulate sperm use, and fertilization failures in worker‐destined eggs are therefore honest signals that workers can use to time queen replacement, which is crucial for colony performance and fitness.

Insights into the molecular basis of long-term storage and survival of sperm in the honeybee (Apis mellifera)

“…With the arrival of sperm in the spermatheca, the conflicts over paternity are largely resolved23 because any further hostility between sperm compromises the fecundity of the queen, which is neither in the interest of queens nor her mates. Competition during egg fertilisation seems largely absent because honeybee queens only use very few sperm to fertilise their eggs, enabling them to maximise their lifetime fecundity in the absence of re-mating13. The physiology of stored sperm is therefore expected to change to maximise long-term survival and fertility.…”

“…Although queens never re-mate after they have started to lay eggs, they are capable of building colonies that survive for decades and consist of millions of individuals in some species2. Because queens are ultimately sperm limited, they are required to initially store large numbers of sperm and use them over prolonged periods of time to economically fertilise large numbers of eggs111213. Such exceptional demands on sperm number and quality also impact social insect males, and some are known to produce exceptionally large ejaculates containing sperm of maximal quality1415.…”

Sperm limitation affects sex allocation in a parasitoid wasp Nasonia vitripennis

“…The observed biased sex ratio can be the result of a physiological constraint related to sperm limitation. For example, in honeybees, queens with a low number of spermatozoa left in their spermatheca are forced to lay unfertilized eggs, which are considered as an honest signal for workers to replace them in the colony (Baer et al, 2016). In N. vitripennis, females are likely to use all the spermatozoa stored in their spermathecal to the very last, as observed in other Pteromalidae, Dinarmus basalis (Chevrier & Bressac, 2002).…”

“…However, the dynamic of spermatozoa release from the spermatheca may depend on their remaining quantity. Indeed, in wasps, the spermathecal pump consists of a sphincter of concentric muscle fibers (Pascini & Martins, 2017), suggested to be involved in controlling the release of spermathecal content during fertilization (Baer et al, 2016). At the time of fertilization, muscle fibers of the sphincter relax allowing the release of sperm into the oviduct where fertilization occurs (Pascini & Martins, 2017).…”

Sperm storage reduces the strength of the mate‐finding Allee effect

“…It plays an important role in species reproduction in which male and female cycles do not coincide (Roques, Díaz-Paniagua, Portheault, Pérez-Santigosa, & Hidalgo-Vila, 2006) as it allows fertilization without the need to mate immediately prior to reproduction (Pearse, Janzen, & Avise, 2002;Roques, Díaz-Paniagua, & Andreu, 2004). This reproductive adaptation is found in a wide range of animals: insects, arachnids, fishes, reptiles, birds, or mammals (Aral & Sahin, 2015;Baer, Collins, Maalaps, & den Boer, 2016;Fromhage, Jennions, & Kokko, 2016). The viability of stored sperm varies from hours to days (in mammals, including humans), and even for years (Holt & Fazeli, 2016), and is especially long-lasting in reptiles (Cutuli, Cannicci, Vannini, & Fratini, 2013).…”