How do fleas mate?

Summary

Fleas must feed and mate to successfully reproduce. Finding a mate and subsequent copulation occurs on the host. Mating begins around 24 hours after the first blood-feeding. The event lasts for 2 to 157 minutes, with a mean duration of 60 minutes for the first mating. To reach maximum fertility, the females must mate with multiple male partners.

Details

Sexual Reproduction

Fleas don’t reproduce asexually. Females must mate to lay fertile eggs. Virgins can lay non-viable eggs. Upon mating, eggs become viable and output quadruples. Virgins’ ability to lay non-viable eggs may be an evolutionary step towards asexual reproduction. Sexual reproduction is believed to be a primitive insect trait.

Anautogeny

Cat fleas are anautogenous, meaning a blood meal is required before they can mate and lay eggs. Unfed fleas can’t mate. They won’t even try. Mating begins after 24 hours of blood-feeding. Males will attempt to mate after eating. However, the most mating pairs occur when both sexes have fed. Mating ceases if the blood supply is removed, but will continue within 15 minutes when it’s reintroduced.

Males

Testicular Plugs

Unfed males have a testicular plug which blocks sperm passage from the testes. This plug must be dissolved before females can be inseminated. A males with an intact plug won’t even attempt to mate. The plug dissolves within 24 hours of the first blood meal. He’ll inseminate several females soon after.

In one study, males completed sperm transfer within 2 hours of feeding, and most females were inseminated by the 8th hour. This shorter time may be explained by the fleas feeding from a host, and not an in vitro system.

Starvation

Starved males (or those fed a protein-free diet) can’t inseminate females. With depleted body fat reserves, the males lack energy for seeking out and mating with a partner. Continuous blood-feeding is required for optimal rates of mating and insemination.

Temperature

Sperm transfer accelerates when fleas are exposed to temperatures of their preferred host animal. It completes at least three times faster at 98.6°F (37°C) than at 77°F (25°C).

Sperm Motility

When male fleas emerge as adults, spermatogenesis has been completed and the sperm are mature. However, the sperm of unfed males are non-motile and enveloped in a gelatinous mass. After 24 hours of feeding, the sperm tails are at peak motility.

Females

Ovary Maturation

Females must be receptive for insemination before mating can be successful. This occurs after 24 hours of feeding on a host. Unfed females can’t produce eggs. Their ovaries are underdeveloped and blocked by a follicular plug. Consuming a blood meal triggers sexual maturation. Once their ovaries have matured, they can begin producing eggs (non-viable until they mate).

Abdomen Distension

The extension of a female’s abdomen, affected by feeding, determines if males can successfully copulate with her. The most success occurs with engorged females, with fully distended abdomens. Males can sometimes mate with 1-day-old unfed females, because their abdomens haven’t fully shrunken yet. However, by the 4th day of starvation, mating attempts aren’t possible.

Starvation

Along with having distended abdomens, females must also continually feed in order to lay eggs. Blood-feeding provides them with necessary nutrients and keeps their metabolism in balance.

Where Fleas Mate

Cat fleas are permanent ectoparasites. They live, feed, mate, and lay eggs on their host. Mating has never been observed off-host, even in close proximity to a cat. Fleas require a blood meal and warm surface temperature before they can mate. Thus, it’s highly unlikely for mating to occur off-host. Also, males and females are most likely to find each other on an animal.

Temperature

Temperature is a critical factor in mating behavior. Copulation only occurs on a surface temperature near that of a host animal, 93.2°F to 107.6°F (34°C to 42°C). In one study, no females were inseminated at 77°F (25°C), while 35% were at 98.6°F (37°C). The optimal temperature occurs at 100.4°F (38°C), which is about the body temperature of cats and dogs.

Protogyny

Most insects exhibit protandry (males mature before females). However, cat fleas belong to a much smaller group of protogynous insects (females mature before males). Female cat fleas emerge as adults 2.7 days sooner than males. This may serve to prevent inbreeding within the same cohort.

Protogny often occurs in species where females mate with multiple partners. The last male’s sperm is used for fertilization (sperm precedence). Since males emerge later, they must mate as many times as other males, competing to displace rival sperm to ensure their genes pass on to the next generation.

Sex Ratios

Females usually predominate in ectoparasite populations. The sex ratio of newly emerged cat fleas is nearly 1:1. However, males have a shorter life span. Thus, the sex ratio of on-host flea populations is 1:3 to 1:5 (M:F). One study showed that 75-85% of fleas on pets are females.

The number of males peaks a month before flea season. This is when there’s the highest occurrence of females mating with multiple partners. And multiple partners results in the highest fertility. However, more males means more harassment between rivals, which could decrease the female’s reproductive success.

Genital Structures

Flea genitals reside on the last three abdominal segments. These genital segments are modified together, looking like one segment. The sensilium (pygidium) is one of the more prominent features. It’s found on the posterior and is covered with circular trichobothria (depressions), each containing a long seta (bristle). It may be sensitive to ultrasonic waves or play a sensory role in mating.

Male Genitals

Genitalia of male fleas have been described as the most elaborate in the animal kingdom. They are highly modified structures with many useful features. On the exterior, there’s a protective a shield to protect the organs, and a movable clasper that attaches to females. Located within the abdominal cavity are the aedegal apodeme (penis plate) and extendable penis rods, which are coiled and retracted within a structure called the endophallic sac. The penis is so thin and wispy, that it can’t enter the female without support by the rods.

Female Genitals

Female genitals aren’t as highly modified as the male’s. The most obvious female structure is the spermatheca, which is where sperm is stored after mating. A sclerotized tube connects the spermatheca with the bursa copulatrix (depression that receives the male organ).

Finding Mates

Adult fleas remain on their acquired host. As a result, males and females are most likely to encounter each other on the host’s body. To find mates, it’s believed that males use their antennae to receive chemical information from females. Before mating, a male will erect his antennae from their grooves and push them against encountered females.

Males of some species use their maxillary palps to detect pheromones from a female’s abdominal cuticle. Rabbit fleas can follow airborne scent. But these behaviors aren’t seen with cat fleas. Female cuticle pheromones don’t produce a mating response. However, males do respond to female extract, indicating that active compounds do exist to mediate attraction. Exactly how male cat fleas find females within dense host hair remains unclear.

When Mating Begins

Once fleas acquire a host, feeding begins within seconds. Mating then occurs in 8 to 24 hours, with most females being mated by 34 hours. They’ll start laying eggs within 24 to 48 hours of acquiring a host.

Mating Act

Males Approaching Females

Males display the first mating behavior. With erect antennae, a male will move towards a female until their heads contact each other. Then, from behind, with his head lowered, he’ll push the female’s abdomen up until he’s underneath her. His posterior will raise. During this, the female continues feeding. If she’s receptive, she’ll accept subsequent male courtship. If she’s unreceptive, she’ll either walk away or raise her hind end.

Males Grasping Females

Mating begins once the male attaches his erect antennae and claspers to the female’s abdomen. The claspers remain attached until copulation ends.

Male antennae are longer than females. The inner surfaces contain suckers for holding onto females. In some species, males don’t loosen the antennal hold until mating ends. However, cat fleas retrieve their antennae immediately after genital linkage. If the female moves her body, or another male disturbs the mating, then the antennae may temporarily be re-erected to grip and control the female.

Instead of using their antennae, male cat fleas primary use their legs to restrain females. They’ll grasp onto the female’s legs with their claws. Their appendages remain interlocked until mating ends.

Genital Linkage

After grasping the female, the male lifts the posterior of his abdomen, causing his body to curve upwards Img 1. He’ll direct his genitals towards the female’s. The aedeagus (insect penis) is then erected to search for the female’s vaginal opening. If he fails, he’ll re-position himself closer to the female and search again.

The female may reject the male by walking or jumping away. In some species, females reject males by kicking. Males occasionally give up the mating attempt, even if no rejection behavior was observed.

If not rejected, the male may successfully insert his aedeagus into the female. The aedeagus’ dorsal lobe reaches the vagina, while the two penis rods penetrate deeper. The thicker rod only reaches the bursa copulatrix, while the thinner one enters the spermathecal duct. Exactly how sperm is transferred into the spermatheca is unknown. The thinner rod’s end is shaped like a cobra head. It’s function may be to convey sperm, or it may scoop out the rival males’ sperm.

With rhythmic contraction and relaxation, the male performs regular strokes of his posterior abdomen (terminalia) against the female. The female continues to feed and excrete feces while mating.

How Mating Ends

Terminating Mating

Mating is generally terminated by the male. He’ll loosen his grasp, lower his abdomen to unlink their genitalia, and then walk away. Finally the claspers to their normal position. He’ll then go find another mate or stop to feed. The female will continue to feed.

Disturbed Mating

Rival males frequently disturb mating pairs. The rival uses his head to push the copulating male’s head from the side. A strong male may successfully displace the mating male, then having a chance to mate with the female. Once interrupted, the female may re-mate with the same male, or she may choose a different mate.

The female sometimes ends copulation by moving away and escaping the male’s grasp. This usually occurs when she’s disturbed by external stimuli, such as other fleas or a sudden increase in light intensity. The abandoned male will try to resume mating, or will go find a different female.

Post-Mating Behavior

A male will display characteristic post-mating behavior. First, he’ll bend his abdomen to the side to clean his terminalia with his hind legs’ spines. Then he’ll replicate the action on the other side. Afterwards, he’ll rub his two hind legs together under his abdomen. This process is repeated several times.

The second step involves cleaning the antennae. He’ll use the claws on his foremost legs to simultaneously scratch the antennal grooves with the antennae inside.

Lastly, the aedeagus is cleaned. He raises his claspers, and withdraws his aedeagus. This in-and-out behavior is repeated a few times until an unidentified, transparent, jelly-like object is finally left outside.

Mating Duration

Cat flea matings can be lengthy, ranging from 2 to 157 minutes. The average is 60 minutes for the first mating, and 40 minutes for the second. One study confined fleas to cells with specific sex ratios. With 1 male and 5 females, each mating lasted 1 to 26 minutes, with an average of 6.6 minutes. With 5 males and 1 female, matings were 1 to 53 minutes long, with an average of 11.1 minutes.

Another study found mating lasts an average of 71.83 minutes when terminated by the male, while only lasting 12 minutes when terminated by the female. Which gender terminates copulation may affect the fertility of the female. Cryptic female choice may be involved with female-terminated matings. Impotent matings are significantly briefer than potent matings, and most of the impotent matings are terminated by females. Females may block sperm transfer because she finds fault with the male’s genitalia.

Multiple Partners

Females must mate multiple times to reach maximum fertility. After the first mating, only 44% of eggs are viable. 71.4% are fertile after the second mating. Multiple matings also increase the overall number of eggs laid. Twice-mated females lay 2.7 times more eggs than once-mated females. And multiple-mated females lay 6.5 times more eggs than once-mated females. Fertility (viable eggs) in twice-mated females is 2.3 times more than once-mated females. And in multiple-mated females, there’s a 9.6-fold increase in fertility over once-mated females.

Females will mate with several males within the first 24 hours on a host. Their spermatheca acquires progressively more sperm during those 24 hours. As many as 48 mating events were observed for one male during an 8 hour period. And one female was observed to mate 27 times within 7 hours.

Once-mated females can lay viable eggs for 3.7 days, and twice-mated females for 4.7 days. This suggests that low numbers of sperm are transferred, or that their longevity is short. When females remain with males and continue to mate, viable eggs are produced until after the males die. Females stop laying viable eggs within 7 days of males being absent. Fertility is restored when males are reintroduced. Male ejaculation may contain oviposition stimulants. Alternatively, females may reabsorb ova when sperm supply is insufficient. The unfertilized eggs could be metabolized and reused later.

Males and females can mate repeatedly with the same partner or different ones. However, there may be a preference for the females to mate with more than one male. Females may gain nutrients, oviposition stimulants, and fresh viable sperm during each additional copulation. This would enhance their reproductive success, and increase the genetic diversity and viability of their offspring. Mating with multiple partners also has disadvantages, such as more energy expenditure and a higher risk of predation.

References