• Birds

• Forced extra-pair copulation

Wysocki D (2025) Drivers of Forced Extra-Pair Copulation in Birds. JSM Sexual Med 9(1): 1148.

In many animals, forced copulation is a severe manifestation of sexual conflict. The most widely accepted explanation for forced copulations in birds is that they enhance the probability of fertilisation success for males. However, at least seven other explanations for this phenomenon have been proposed in recent years. Increased fertilisation success appears to apply primarily to species possessing a penis. In other birds, in which the probability of fertilisation is low, the principal function of forced extra-pair copulation (FEPC) seems to be the creation of a landscape of fear, which may reduce competition for local resources. Additionally, FEPC may fulfill other species-specific roles unrelated to these general functions.

FEPC: Forced Extra-Pair Copulation; EPP: Extra-Pair Paternity; IFE: Immediate Fertilisation Enhancement; CODE: Creation of a Dangerous Environment

The realisation that male and female genomes are in conflict has revolutionised our interpretation of interactions between the sexes and confirmed that sexual conflict is a powerful evolutionary driver [1]. In many animals, forced copulation is a severe manifestation of this conflict [2-4]. The most common explanation for forced copulations in birds is that they increase the probability of fertilisation success for males — the Immediate Fertilisation Enhancement (IFE) hypothesis [5]. Many behavioural ecologists regard FEPC as a regular secondary reproductive tactic employed by male birds [6]. It is supported by studies reporting that FEPC attempts peak in frequency during the egg laying period and tend to be directed at fertile females, strongly suggesting that males pursue FEPC to inseminate more females [see 7 for review].

Moreover, contemporary research suggests that, in waterfowl, both penis and vaginal morphology variability (such as dead-end sacs and clockwise coils, which seem to serve to eliminate the intromission of the anticlockwise spiralling male phallus without female cooperation) are related to the frequency of FEPC within species and that females have evolved a hidden anatomical choice mechanism in response to forced extra-pair copulations [8]. These adaptations are likely to contribute to the generally low efficiency (i.e., siring success) of FEPC [8]. However, only about 3% of bird species possess a penis, including ratites (order Struthioniformes), tinamous (family Tinamidae), cracids (family Cracidae), screamers (family Anhimidae), the magpie goose (Anseranas semipalmata), and waterfowl [9].

In species lacking a penis, insemination requires female cooperation [10], therefore making the occurrence of FEPC in such species puzzling [11]. In recent years, several additional hypotheses have been proposed to explain FEPC in birds [12,13]. In this article, I evaluate these hypotheses using species whose biology is relatively well understood.

There are several different, non-mutually exclusive explanations for the evolution and maintenance of FEPC:

1. The Immediate Fertilisation Enhancement (IFE) hypothesis posits that FEPC is maintained by selection due to its role in directly enhancing fertilisation success [5,6].

2. The relic hypothesis suggests that FEPC is an evolutionary relic. Although it may have ancestrally provided paternity benefits (due to the occurrence of a penis in ancestral birds), it now persists as a non-adaptive, vestigial behaviour [12].

3. FEPC may be a pleiotropic by-product of other traits that are selectively advantageous to males [3]. For example, high testosterone levels, which may increase male attractiveness, are also associated with hypersexual behaviour, potentially resulting in FEPC [15].

4. The ‘Creation of a Dangerous Environment’ (CODE) hypothesis [16] proposes that males collectively create a hostile environment for females by subjecting them to sexual harassment. This alters female behaviour, restricting their reproductive choices and making them more easily controlled by their “protective” mates.

5. The ‘territory signalling’ hypothesis [12] suggests that FEPC serves a territorial function, where males attempt to claim future breeding sites by forcing copulations with resident females and signalling through loud copulatory calls.

6. The ‘reproductive suppression’ hypothesis [17] proposes that FEPC may suppress a victim female’s reproductive success through the long-term physiological effects of stress on incubation or nestling-rearing behaviour. In such cases, paired males may use FEPC to reduce the reproductive success of neighbouring pairs, thereby decreasing competition for resources.

7. The deterrence hypothesis [13] suggests that FEPC serves primarily as an aggressive act rather than one driven by sexual interest. Neighbouring males may target the weaker member of a pair to deter rivals.

8. The sperm turnover hypothesis posits that, similar to masturbation, FEPC may be used to expel inferior sperm, thus improving subsequent sperm quality [18].

Most of these hypotheses are extremely difficult to evaluate, as they require detailed knowledge of speciesspecific behaviour. Furthermore, many have been proposed based on observations in only a few species. To date, only the IFE hypothesis is well documented across a broad range of bird species. The presence of a phallus may enable males to achieve intromission without female cooperation, thereby increasing their likelihood of fertilisation and providing them with a copulatory advantage over females [19].

In waterfowl (Anatidae), FEPC has been recorded in 55 species across 17 genera, accounting for about one-third of all species in this group [20]. This is the best-studied group of birds with a copulatory organ, where fertilisation as a result of FEPC has been documented [8]. In other avian taxa, fertilisation through FEPC also appears possible. For example, in the wandering albatross (Diomedea exulans) [21], extra-pair copulations may benefit unpaired males while occurring randomly in females, supporting the idea that EPP may result solely from forced copulations.

Similarly, genetic data for the New Zealand stitchbird (Notiomystis cincta) suggest that sexual coercion is successful in achieving extra-pair fertilisation. In this species, sexually active males develop an extremely large cloacal protuberance, which swells by almost 400% during the breeding season, functioning similarly to an intromittent organ and enabling forced copulation [22]. Forced fertilisation may also occur in species such as the purple martin (Progne subis) [23] and razorbill (Alca torda) [24].

However, female cooperation in these cases does not necessarily imply an absence of male coercion. In many species, females may tolerate EPC attempts to minimise harassment or avoid injury [25]. The relic hypothesis remains plausible, as FEPC occurs in numerous passerine species where fertilisation via forced copulation is unlikely [11]. It therefore cannot be ruled out that FEPC is a relic behaviour, although limited knowledge of the species’ biology may hinder the proposal of alternative explanations.

The pleiotropic by-product hypothesis is supported by findings in mallards (Anas platyrhynchos), where high testosterone levels correlate with both FEPC and the amount of time males spend associating with females [26]. Thus, elevated testosterone may also promote FEPC in other species. Several hypotheses suggest that FEPC is selectively favoured despite not directly enhancing fertilisation success. The CODE hypothesis, originally hinted at by Heinroth [27] and later formalised by Gowaty and Buschhaus [16], proposes that sexual violence by males creates a hostile environment, restricting female reproductive autonomy.

However, studies on passerines such as the stitchbird [22], jackdaw [12], and blackbird [13] suggest that the CODE hypothesis does not adequately explain FEPC in these species. The territory signalling hypothesis [17], proposed for jackdaws, posits that FEPC serves to signal territory claims. To date, this explanation has been suggested only for this species. The reproductive suppression hypothesis [17] suggests that FEPC reduces female reproductive success through stress, thereby reducing local competition. Similarly, the deterrence hypothesis proposes that FEPC is primarily aggressive, targeting weaker rivals to deter potential competitors [13].

At a proximate level, both the reproductive suppression and deterrence hypotheses imply that forced copulations may elevate female corticosteroid levels and contribute to a ‘landscape of fear’, similar to the threat posed by predators. This is supported by observations in the New Zealand stitchbird, where harassment during egg formation alters female foraging behaviour and reduces nutrient intake [28]. The sperm turnover hypothesis suggests that FEPC may improve sperm quality by expelling older, less viable sperm [18].

For instance, in black-legged kittiwakes (Rissa tridactyla), fertilisation with older sperm is associated with lower hatching success and chick quality [29]. Therefore, in some species, FEPC may facilitate the removal of old sperm. However, in many bird species, including blackbirds, males also copulate with surrogate objects [30]. Copulations with fledglings, moss, or sticks may offer a less costly but equally effective means of eliminating inferior sperm.

Based on current knowledge, FEPC appears to serve two primary functions. The first, mainly concerning birds with a penis, is to increase male reproductive success. The second involves creating a ‘landscape of fear’ that reduces local reproductive competition. Additionally, in some species, FEPC may serve other roles unrelated to these two functions, as suggested by the territory signalling hypothesis.

The author is grateful to all the students and volunteers for their help with the fieldwork. Co-financed by the Minister of Science under the “Regional Excellence Initiative” Program for 2024-2027 (RID/SP/0045/2024/01).

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