Reproductive interference is the interaction between individuals of different species during mate acquisition that leads to a reduction of fitness in one or more of the individuals involved. The interactions occur when individuals make mistakes or are unable to recognise their own species, labelled as ‘incomplete species recognition'. Reproductive interference has been found within a variety of taxa, including insects, mammals, birds, amphibians, marine organisms, and plants. [1]
There are seven causes of reproductive interference, namely signal jamming, heterospecific rivalry, misdirected courtship, heterospecific mating attempts, erroneous female choice, heterospecific mating, and hybridisation. All types have fitness costs on the participating individuals, generally from a reduction in reproductive success, a waste of gametes, and the expenditure of energy and nutrients. These costs are variable and dependent on numerous factors, such as the cause of reproductive interference, the sex of the parent, and the species involved. [1]
Reproductive interference occurs between species that occupy the same habitat and can play a role in influencing the coexistence of these species. It differs from competition as reproductive interference does not occur due to a shared resource. [1] Reproductive interference can have ecological consequences, such as through the segregation of species both spatially and temporally. [2] It can also have evolutionary consequences, for example; it can impose a selective pressure on the affected species to evolve traits that better distinguish themselves from other species. [3]
Reproductive interference can occur at different stages of mating, from locating a potential mate, to the fertilisation of an individual of a different species. There are seven causes of reproductive interference that each have their own consequences on the fitness of one or both of the involved individuals. [1]
Signal jamming refers to the interference of one signal by another. [1] Jamming can occur by signals emitted from environmental sources (e.g. noise pollution), or from other species. In the context of reproductive interference, signal jamming only refers to the disruption of the transmission or retrieval of signals by another species. [1] The process of mate attraction and acquisition involves signals to aid in locating and recognising potential mates. Signals can also give the receiver an indication of the quality of a potential mate. [4] Signal jamming can occur in different types of communication. Auditory signal jamming, otherwise labelled as auditory masking, is when a noisy environment created by heterospecific signals causes difficulties in identifying conspecifics. [5] Likewise in chemical signals, pheromones that are meant to attract conspecifics and drive off others may overlap with heterospecific pheromones, leading to confusion. [6] Difficulties in recognising and locating conspecifics can result in a reduction of encounters with potential mates and a decrease in mating frequencies. [6]
Vibrational signalling in the American grapevine leafhopper - Individuals of the American grapevine leafhopper communicate with each other through vibrational signals that they transmit through the host plant. American grapevine leafhoppers are receptive of signals within their receptor’s sensitivity range of 50 to 1000 Hz. The vibrations can be used to identify and locate potential female mates. To successfully communicate, a duet is performed between the male and female American grapevine leafhopper. The female replies within a specific timeframe after the male signal, and the male may use the timing of her reply to identify her. However, vibrational signals are prone to disruption and masking by heterospecific signals, conspecific signals, and background noise that are within their species-specific sensitivity range. The interference of the duet between a male and female American grapevine leafhopper can reduce the male’s success in identifying and locating the female, which can reduce the frequency of mating. [7]
Auditory signalling in the gray treefrog (Hyla versicolor) and the Cope's gray treefrogs (Hyla chrysoscelis) – The success of reproduction is dependent on a female’s ability to correctly identify and respond to the advertisement call of a potential mate. At a breeding site with high densities of males, the male’s chorus may overlap with heterospecific calls, making it difficult for the female to successfully locate a mate. When the advertisement calls of the male gray treefrog and male Cope’s gray treefrog overlap, female gray treefrogs make mistakes and choose the heterospecific call. The amount of errors the female makes is dependent on the amount of overlap between signals. Female Cope’s gray treefrogs can better differentiate the signals and are only significantly affected when heterospecifics completely overlap conspecific male signals. However, female Cope’s gray treefrogs prefer conspecific male signals that have less overlap (i.e. less interference). Furthermore, females have longer response times to overlapped calls, where it takes longer for them to choose a mate. Signal jamming can affect both males and females as difficulties in identifying and locating a mate reduces their mating frequencies. Females may have more costs if they mate with a male of a lower quality, and may be susceptible to a higher risk of predation by predators within the breeding site if they take longer to choose and locate a male. Heterospecific mating between the gray treefrog and Cope’s gray treefrogs also can form an infertile hybrid which is highly costly to both parents due to the wastage of gametes. [8]
Chemical signalling in ticks – Female ticks produce a pheromone that is a species-specific signal to attract conspecific males that are attached to the host. Female ticks also produce a pheromone that is not species-specific which can attract males that are in a close proximity to her. Pheromones emitted from closely related species can mix and lead to interference. Three species of ticks: Aponomma hydrosauri, Amblyomma albolimbatum, and Amblyomma limbatum, are closely related and can interfere with one another when attached to the same host. When two of the species of tick are attached on the same host, males have difficulties locating a female of the same species, potentially due to the mixing of pheromones. The pheromone that is not species-specific also has the capability of attracting males of all three species when they are in close proximity to the female. The presence of a heterospecific female can also reduce the time a male spends with conspecific females, leading to a reduction of reproductive success. Furthermore, when Amblyomma albolimbatum males attach to Aponomma hydrosauri females to mate, despite being unsuccessful, they remain attached which physically inhibits following males from mating. [9]
Heterospecific rivalry occurs between males, when a male of a different species is mistaken as a rival for mates (i.e. mistaken for a conspecific male). [1] In particular, heterospecific rivalry is hard to differentiate from other interspecific interactions, such as the competition over food and other resources. [1] Costs to the mistaken males can include the wastage of time and energy, and a higher risk of injury and predation if they leave their mating territory to pursue the heterospecific male. [10] Males that chase off a heterospecific male may also leave females exposed to following intruders, whether it be a conspecific or heterospecific male. [10]
Eastern amberwing dragonfly ( Perithemis tenera ) – Male Eastern amberwing dragonflies are territorial as they defend mating territories from rival conspecific males. The male will perch around their territory and pursue conspecifics that fly near the perch. When the male is approached by a species of horsefly and butterfly, they are similarly pursued. The horsefly and butterfly do not compete over a common resource with the Eastern amberwing dragonfly, have not been seen interfering with the mating within the territory, and are neither a predator nor prey of the Eastern amberwing dragonfly. Instead, they are pursued potentially due to being mistaken for a rival conspecific as they share similar characteristics in size, colour, and flight height. The similar characteristics may be cues used by the male Eastern amberwing dragonfly to identify conspecifics. The heterospecific pursuit is costly for the male as they waste energy and time, have a higher risk of injury, and may lose opportunities to defend their territory against subsequent intruders. [11]
Misdirected courtship occurs when males display courtship towards individuals of a different species of either sex. [1] The misdirection is caused by a mistake during species recognition, or by an attraction towards heterospecifics that possess desirable traits. [1] Such desirable traits are those traits that normally are an indicator of conspecific mate quality, such as body size. [12] Costs associated with misdirecting courtship for males include the wasted energy investment in the attempt to court heterospecifics, and a decrease in mating frequency within species. [13]
Waxbill – Waxbills are monogamous, where an individual only has one partner. Parents also display biparental care, where both the mother and father contribute to the care of the offspring. The combination of monogamy and biparental investment suggest that both male and female waxbills should be ‘choosy’ and have strong preferences to reduce the chances of mating with a heterospecific female. Males of the three species of waxbill: blue breast (Uraeginthus angolensis), red cheek (Uraeginthus bengalus), and blue cap (Uraeginthus cyanocephalus), have differing strengths of preferences for conspecific females when also presented with a heterospecific female. The differing preferences is affected by the body size of the females, potentially due to body size being an indicator of fecundity, which is the ability to produce offspring. Blue breast males prefer conspecifics over red cheek females that are smaller; however, have a weaker preference for conspecifics over blue breast females that are only slightly smaller. Red cheek males have no preference for conspecifics in the presence of a larger blue breast female or blue cap female. Blue cap males prefer conspecifics over red cheek females; however, have no preference for conspecifics in the presence of a larger blue breast male. [14]
Atlantic salmon (Salmo salar) – Atlantic salmon that were once native to Lake Ontario were reintroduced to the lake to study their spawning interactions with other species of fish, including the chinook salmon, coho salmon, and brown trout. Chinook salmon interacted with Atlantic salmon the most, where male chinooks attempted to court female Atlantic salmon. Male chinooks also chased away, and in some interactions, behaved aggressively towards other Atlantic salmon that approached female Atlantic salmon. A male brown trout was also observed to court a female Atlantic salmon. Misdirected courtship towards the Atlantic salmon can cause problems in waters that the Atlantic salmon currently occupy, and towards conservation efforts to reintroduce the Atlantic salmon to Lake Ontario. Implications of misdirected courtship on the Atlantic salmon can cause the delay or prevention of spawning, and the hybridisation of the Atlantic salmon with other species. [15]
Heterospecific mating attempts occur when males attempt to mate with females of a different species, regardless of whether courtship occurs. [1] During each mating attempt, sperm transfer may or may not occur. [1] Both sexes have costs when a heterospecific attempts to mate. Costs associated with heterospecific mating attempts include wasted energy, time, and potentially gametes if sperm transfer occurs. [16] There is also a risk of injury and increased risk of predation for both sexes. [16]
Cepero's grasshopper (Tetrix ceperoi) and the slender groundhopper (Tetrix subulata) – Naturally the distribution of the Cepero’s grasshopper and slender groundhopper overlap; however, they rarely co-exist. The reproductive success of the Cepero’s grasshopper decreases when housed within the same enclosure as high numbers of the slender groundhopper. The reduction of reproductive success stems from an increase in mating attempts by the Cepero's grasshopper towards the slender groundhopper, which may be due to their larger body size. However, these mating attempts are generally unsuccessful as the mate recognition of female slender groundhoppers are reliable, which may be due to the different courtship displays of the two species. The reduced reproductive success can cause the displacement in one of the species, potentially a factor as to why the species rarely co-exist despite sharing similar habitat preferences. [17]
Italian agile frog (Rana latastei) - The distribution of Italian agile frog and the agile frog (Rana dalmatina) overlap naturally in ponds and drainage ditches. In the areas of overlap, the abundance of agile frogs is higher than Italian agile frogs. When there is a higher abundance of agile frogs, the mating between Italian agile frogs is interfered with. Male agile frogs attempt to displace male Italian agile frogs during amplexus, which is a type of mating position where the male grasps onto the female. The Italian agile frog and agile frog have been seen in amplexus when co-existing. The mating attempts by the agile frog reduces the reproductive success of the Italian agile frog. The Italian agile frog also produces a lower number of viable eggs in the presence of the agile frog, potentially due to sperm competition between the male Italian agile frog and agile frog. [18]
Species and sex-recognition errors among true toads are very well studied. [19] [20] Toads are known to have amplexus with species from other genera in the same family, [21] and species belonging to other families. [22] Hybridization cases have also been reported among toads. [23]
Erroneous female choice refers to mistakes made by females when differentiating males of the same species from males of a different species. [1] Female choice may occur at different stages of mating, including male courtship, copulation, or after copulation. [24] Female choice can depend on the availability of appropriate males. [25] When there are less available conspecific males, females may make more mistakes as they become less ‘choosy’. [25]
Striped ground cricket ( Allonemobius fasciatus ) and Southern ground cricket ( Allonemobius socius ) - The striped ground cricket and the Southern ground cricket are closely related species that have an overlapping distribution. Both crickets use calling songs in order to identify and locate potential mates. The songs of the two species have a different frequency and period. Females of both species show little preference between the songs from conspecific and heterospecific males. The minor preference disappears if the intensity of the calls are altered. The lack of ability to differentiate between the two songs can result in erroneous female choice. Erroneous female choice has costs, including energy wastage, and increases in predation risk when searching for a conspecific. Additionally, it is highly costly when the mistake leads to heterospecific mating, which involves the wastage of gametes. However, the cost of erroneous female choice may be small for the striped ground and Southern ground cricket due to their high abundance. The lack of ability to differentiate between the calling songs is proposed to be due to the weak selective pressure on the females. [26]
Heterospecific mating is when two individuals from different species mate. After the male transfers his sperm into the heterospecific female, different processes can occur that may change the outcome of the copulation. Heterospecific mating may result in the production of a hybrid in some pairings. Costs associated to heterospecific mating include the wastage of time, energy, and gametes. [1]
Spider mites – two closely related Panonychus mites: the Panonychus citri and Panonychus mori, are generally geographically segregated and on occasion co-exist. However, the co-existence is not stable as the Panonychus mori is eventually excluded. The exclusion is a result of reproductive interference and also due to the higher reproductive rate of the Panonychus citri. Heterospecific mating occurs between the two species which can produce infertile eggs or infertile hybrid females. Furthermore, females are not able to produce female offspring after mating with a heterospecific. In addition to the wastage of energy, time, and gametes, the inability to produce female offspring after heterospecific mating skews the sex ratio of the co-existing populations. The high costs associated with heterospecific mating along with the higher reproductive rate of the Panonychus citri lead to the displacement of the Panonychus mori. [27]
Black-legged meadow katydid (Orchelimum nigripes) and the handsome meadow katydid (Orchelimum pulchellum) – The two closely related species of katydid have the same habitat preferences and co-exist along the Potomac River. Females of both species that mate heterospecifically have a large reduction in fecundity compared to conspecific pairings. Heterospecific mating either produces no eggs or male hybrids that may be sterile. Both individuals suffer a large fitness cost from the wastage of energy, time, and gametes, as they unsuccessfully pass on their genes. However, females may be able to offset this cost through multiple mating, as they receive nutritional benefits from consuming a nuptial food gift from the male, otherwise known as the spermatophylax. [28]
Hybridisation, in the context of reproductive interference, is defined as the mating between individuals of different species that can lead to a hybrid, an inviable egg, or an inviable offspring. [29] The frequency of hybridisation increases if it is hard to recognise potential mates, especially when heterospecifics share similarities, such as body size, [30] colouration, [31] and acoustic signals. [32] Costs associated with hybridisation are dependent on the level of parental investment and on the product of the pairing (hybrid). [1] Hybrids have the potential to become invasive if they develop traits that make them more successful than their parent species in surviving within new and changing habitats, otherwise known as hybrid vigor or heterosis. [33] Compared to each individual parent species, they hold a different combination of characteristics that can be more adaptable and 'fit' within particular environments. [34] If an inviable product is produced, both parents suffer from the cost of unsuccessfully passing on their genes. [1]
California Tiger Salamanders (Ambystoma californiense) x Barred Tiger Salamanders (Ambystoma mavortium) - California tiger salamanders are native to California, and were geographically isolated from Barred tiger salamanders. [35] Barred tiger salamanders were then introduced by humans to California, and the mating between these two species led to the formation of a population of hybrids. [35] The hybrids have since established in their parent habitat and spread into human modified environments. [35] Within hybrids, the survivability of individuals with a mixed-ancestry is higher than individuals with a highly native or highly introduced genetic background. [36] Stable populations can form as populations with a large native ancestry become mixed with more introduced genes, and vice versa. [36] Hybrids pose both ecological and conservation consequences as they threaten the population viability of the native California tiger salamanders, which is currently listed as an endangered species. [37] The hybrids may also affect the viability of other native organisms within the invaded regions, as they consume large quantities of aquatic invertebrate and tadpole. [36]
Red deer (Cervus elaphus) x sika deer (Cervus nippon) - The sika deer were originally introduced by humans to Britain and has since established and spread through deliberate reintroductions and escape. The red deer are native to Britain and hybridise with the sika deer in areas which they co-exist. Heterospecific mating between the red deer and sika deer can produce viable hybrids. Sika deer and the hybrids may outcompete and displace native deer from dense woodland. As the complete eradication of sika and the hybrids is impractical, management efforts are directed at minimising spread by not planting vegetation that would facilitate their spread into regions where the red deer still persist. [38]
Damselfish are those within the subfamilies Abudefdufinae, Chrominae, Lepidozyginae, Pomacentrinae, and Stegastinae within the family Pomacentridae. Most species within this group are relatively small, with the largest species being about 30cm in length. Most damselfish species exist only in marine environments, but a few inhabit brackish or fresh water. These fish are found globally in tropical, subtropical, and temperate waters.
Hyla is a genus of frogs in the tree frog family Hylidae. As traditionally defined, it was a wastebasket genus with more than 300 species found in Europe, Asia, Africa, and across the Americas. After a major revision of the family, most of these have been moved to other genera so that Hyla now only contains 17 extant (living) species from Europe, northern Africa and Asia. The earliest known fossil member of this genus is †Hyla swanstoni from the Eocene of Saskatchewan, Canada, but its designation to Hyla happened before the major revision, meaning that its position needs confirmation.
Leptidea sinapis, or the wood white butterfly of the family Pieridae, is a small white butterfly that is mainly found in England, Ireland, and Northern Europe. The butterfly has white wings with grey or yellow markings near the center or tip of the wing. It flies slowly and low over its shrubbery habitat. Males initiate courtship with females and can mate multiply, while females tend to only mate once in their lifetime.
The American green tree frog is a common arboreal species of New World tree frog belonging to the family Hylidae. This nocturnal insectivore is moderately sized and has a bright green to reddish-brown coloration. Commonly found in the central and southeastern United States, the frog lives in open canopy forests with permanent water sources and abundant vegetation. The American green tree frog is strictly aquatic during the hibernating and mating seasons. When defending its territory, the frog either emits aggressive call signals or resolves to grapple with intruders, seldom leading to injury or death. To avoid predation, the frog will leap into the water or jump into the treetops.
Hyla japonica, commonly known as the Japanese tree frog, is a species of anuran native to Japan, China, and Korea. H. japonica is unique in its ability to withstand extreme cold, with some individuals showing cold resistance at temperatures as low as −30 °C for up to 120 days. H. japonica are not currently facing any notable risk of extinction and are classified by the IUCN as a species of "least concern". Notably, H. japonica have been sent to space in a study that explored the effect of microgravity on H. japonica. Hyla japonica is synonymous with Dryophytes japonicus.
The gray treefrog is a species of small arboreal holarctic tree frog native to much of the eastern United States and southeastern Canada.
The mechanisms of reproductive isolation are a collection of evolutionary mechanisms, behaviors and physiological processes critical for speciation. They prevent members of different species from producing offspring, or ensure that any offspring are sterile. These barriers maintain the integrity of a species by reducing gene flow between related species.
Podarcis hispanicus, also known as Iberian wall lizard, is a small wall lizard species of the genus Podarcis. It is found in the Iberian peninsula, in northwestern Africa and in coastal districts in Languedoc-Roussillon in France. In Spanish, this lizard is commonly called lagartija Ibérica.
Dryophytes gratiosus, commonly known as the barking tree frog, is a species of tree frog endemic to the south-eastern United States. Formerly known as Hyla gratiosa.
Chrysochus cobaltinus, the cobalt milkweed beetle or blue milkweed beetle, is a member of the diverse family of leaf beetles, Chrysomelidae. It is named after its cobalt-blue exoskeleton, which makes it easy to spot and distinguish, and its tendency to feed off milkweed plants. It occurs in the Western United States and British Columbia.
Spodoptera litura, otherwise known as the tobacco cutworm or cotton leafworm, is a nocturnal moth in the family Noctuidae. S. litura is a serious polyphagous pest in Asia, Oceania, and the Indian subcontinent that was first described by Johan Christian Fabricius in 1775. Its common names reference two of the most frequent host plants of the moth. In total, 87 species of host plants that are infested by S. litura are of economic importance. The species parasitize the plants through the larvae vigorous eating patterns, oftentimes leaving the leaves completely destroyed. The moth's effects are quite disastrous, destroying economically important agricultural crops and decreasing yield in some plants completely. Their potential impact on the many different cultivated crops, and subsequently the local agricultural economy, has led to serious efforts to control the pests.
Allobates femoralis is a species of frog in the family Aromobatidae. It is found in Bolivia, Brazil, Colombia, Ecuador, French Guiana, Guyana, Peru, and Suriname. Its natural habitat is tropical lowland forests.
Dendropsophus ebraccatus, also known as the hourglass treefrog, referring to the golden-brown hourglass shape seen surrounded by skin yellow on its back. Their underbellies are yellow. Their arms and lower legs usually display bold patterns while their upper legs or thighs are light yellow giving them the appearance of wearing no pants. The species name "ebraccata" translates to "without trousers" in Latin.
Engystomops petersi is a species of frog in the family Leptodactylidae. It is found in Amazonian Colombia, Ecuador, and Peru. It is morphologically similar to its sibling species, Engystomops freibergi, and for a period the latter was considered to be a junior synonym of Engystomops petersi. Taxonomy and classification of this species is constantly changing due to the continual evolution of behavioral isolation and rapid speciation in the region. There are also records from the Guianas that have not yet been allocated to either species. Divergence of these two species seems to have been driven by behavioural isolation related to male call characteristics more than geographic isolation.
The Túngara frog is a species of frog in the family Leptodactylidae. It is a small nocturnal terrestrial frog found in Mexico, Central America, and the northeastern regions of South America.
The ocoee salamander is a species of salamander in the family Plethodontidae. This salamander has a variety of colors and patterns, and got its name from Tennessee state wildflower. Its natural habitats are temperate forests, rivers, intermittent rivers, freshwater springs and wet rocks in mountainous areas of the Southeastern United States. It was first described by Nicholls in 1949. They are territorial and feed on small invertebrates. It is widely distributed in the southeastern United States and is listed as "Least Concern" by the International Union for Conservation of Nature.
A courtship display is a set of display behaviors in which an animal, usually a male, attempts to attract a mate; the mate exercises choice, so sexual selection acts on the display. These behaviors often include ritualized movement ("dances"), vocalizations, mechanical sound production, or displays of beauty, strength, or agonistic ability.
A mating call is the auditory signal used by animals to attract mates. It can occur in males or females, but literature is abundantly favored toward researching mating calls in females. In addition, mating calls are often the subject of mate choice, in which the preferences of one gender for a certain type of mating call can drive sexual selection in a species. This can result in sympatric speciation of some animals, where two species diverge from each other while living in the same environment.
Sexual selection in amphibians involves sexual selection processes in amphibians, including frogs, salamanders and newts. Prolonged breeders, the majority of frog species, have breeding seasons at regular intervals where male-male competition occurs with males arriving at the waters edge first in large number and producing a wide range of vocalizations, with variations in depth of calls the speed of calls and other complex behaviours to attract mates. The fittest males will have the deepest croaks and the best territories, with females making their mate choices at least partly based on the males depth of croaking. This has led to sexual dimorphism, with females being larger than males in 90% of species, males in 10% and males fighting for groups of females.
Reinforcement is a process within speciation where natural selection increases the reproductive isolation between two populations of species by reducing the production of hybrids. Evidence for speciation by reinforcement has been gathered since the 1990s, and along with data from comparative studies and laboratory experiments, has overcome many of the objections to the theory. Differences in behavior or biology that inhibit formation of hybrid zygotes are termed prezygotic isolation. Reinforcement can be shown to be occurring by measuring the strength of prezygotic isolation in a sympatric population in comparison to an allopatric population of the same species. Comparative studies of this allow for determining large-scale patterns in nature across various taxa. Mating patterns in hybrid zones can also be used to detect reinforcement. Reproductive character displacement is seen as a result of reinforcement, so many of the cases in nature express this pattern in sympatry. Reinforcement's prevalence is unknown, but the patterns of reproductive character displacement are found across numerous taxa, and is considered to be a common occurrence in nature. Studies of reinforcement in nature often prove difficult, as alternative explanations for the detected patterns can be asserted. Nevertheless, empirical evidence exists for reinforcement occurring across various taxa and its role in precipitating speciation is conclusive.