Heterospecific Females Research Articles

Heterospecific mating and species recognition in the planktonic marine copepods Temora stylifera and T. longicornis

Many planktonic copepods use diffusible pheromone or hydromechanical signals to remotely detect the presence of potential mates. To determine whether these mating signals also play a role in species recognition and mate choice, we observed and video recorded (3D) mate-finding and pursuit behaviors in heterospecific and conspecific mating crosses in a pair of congeneric, partially sympatric species (Temora stylifera and T. longicornis) in the laboratory. The species appear to have asymmetrical pre-mating isolation, with T. longicornis males readily pursuing T. stylifera females to mate contact and capture, but with little mate-finding activity observed in the reverse cross. Males of T. longicornis pursuing heterospecific females executed a number of behaviors known to facilitate successful pheromone trail following and mate capture in conspecific mating, including accelerated swimming in a ‘signal-scanning’ mode to recover a lost pheromone trail, reversal of the tracking direction in cases when the male initiated tracking in the incorrect direction, and accelerated swimming speeds when in the presence of a pheromone signal but prior to locating the trail. Detailed analyses of mate-tracking behavior in T. longicornis male × T. stylifera female crosses gave no indication that males were aware they were pursuing heterospecific females prior to mate contact, indicating that diffusible pheromone and hydromechanical signals are not used, either singly or in combination, for species recognition in this mating pair. Heterospecific mating attempts among sympatric, congeneric copepods may commonly proceed to mate capture, and incur fitness costs to either or both mating partners.

Spatial and behavioural measures of social discrimination by captive male zebra finches: Implications of sexual and species differences for recognition research

All bird species reproduce sexually and individuals need to correctly identify conspecifics for successful breeding. Captive zebra finches are a model system for studying the factors involved in species recognition and mate choice. However, male zebra finches' behavioural responses in a spatial preference paradigm to a range of estrildid finch species, other than domesticated Bengalese finches, remain unknown. We investigated spatial and display responses of male zebra finch subjects to stimulus females between conspecific and four phylogeographically relevant finch species, in addition to female Bengalese finches. Surprisingly, male subjects did not show consistent spatial association with conspecific over heterospecific females. Overall, as predicted by sexual selection theory, the spatial proximity responses of males were less discriminatory compared to female zebra finches' responses tested previously using the same paradigm. However, male subjects showed consistently more behavioural displays towards female conspecifics than heterospecifics which were positively related to the behavioural display rates of the respective female stimuli. Some male behavioural responses, other than song, also showed significant differences between the different stimulus species and consistently differed across individual test subjects, with the most individual subject variation seen in choice trials between female conspecific and Bengalese finch stimuli. The results are important for the design and interpretation of future behavioural and neurobiological experiments on species recognition systems using the zebra finch as a model species.

Learning decreases heterospecific courtship and mating in fruit flies.

Recent theory and data suggest that adaptive use of learning in the context of sexual behaviour could contribute to assortative mating. Experiments examining this issue indicated that male Drosophila persimilis that experienced courtship and rejection by heterospecific females exhibited significantly lower levels of heterospecific courtship and mating compared with those of inexperienced males. These results indicate that experience in the context of sexual behaviour in fruit flies could reduce gene flow between diverging populations, which may contribute to incipient speciation.

Examining the Role of Cuticular Hydrocarbons in Firefly Species Recognition

AbstractDuring animal courtship, multiple signals transmitted in different sensory modalities may be used to recognize potential mates. In fireflies (Coleoptera: Lampyridae), nocturnally active species rely on long‐range bioluminescent signals for species, sex, and mate recognition, while several diurnally active species rely on pheromonal signals. Although in many insects non‐volatile cuticular hydrocarbons (CHC) also function in species and sex discrimination, little is known about the potential role of CHC in fireflies. Here, we used gas chromatography to characterize species and sex differences in the CHC profiles of several North American fireflies, including three nocturnal and two diurnal species. Additionally, we conducted behavioral bioassays to determine whether firefly males (the searching sex) were differentially attracted to extracts from conspecific vs. heterospecific females. Gas chromatography revealed that nocturnal Photinus fireflies had low or undetectable CHC levels in both sexes, while diurnal fireflies showed higher CHC levels. No major sex differences in CHC profiles were observed for any firefly species. Behavioral bioassays demonstrated that males of the diurnal firefly Ellychnia corrusca were preferentially attracted to chemical extracts from conspecific vs. heterospecific females, while males of the remaining species showed no discrimination. These results suggest that while CHC may function as species recognition signals for some diurnal fireflies, these compounds are unlikely to be important contact signals in nocturnal Photinus fireflies.

Divergence in Multiple Courtship Song Traits between Drosophila santomea and D. yakuba

The courtship song of Drosophila is useful for species recognition and sexual selection. A new species of the melanogaster group of Drosophila, D. santomea, has recently been described from the island of Sao Tomein the Gulf of Guinea. We describe the courtship song of D. santomea and compare it with that of its sibling species D. yakuba. Both species have a relatively unusual song pattern for melanogaster-group species, in that they have two types of pulse song but no sine song. There are large dif- ferences in the inter-pulse interval of both types of song, but no major differences in pulse shape or intrapulse frequency between the species. The song of D. yakuba is similar in lines from the African mainland (allo- patric to D. santomea) and from Sao Tome´ (sympatric). We test if song pattern might influence sexual isolation by examining the mating suc- cess of wingless males with homo- and hetero-specific females. We show that song pattern contributes to sexual stimulation, but the differences in song patterns alone are unlikely to explain patterns of sexual isola- tion such as the asymmetrical isolation seen between species.

Interspecific Pheromone Plume Interference Among Sympatric Heliothine Moths: A Wind Tunnel Test Using Live, Calling Females

Three species of North American heliothine moths were used to determine the level at which interspecific female interference of male attraction to conspecific females occurs. We used live calling females of Heliothis virescens, H. subflexa, and Helicoverpa zea, as lures for conspecific males in a wind tunnel, and then placed heterospecific females on either side of the original species such that the plumes of the three females overlapped downwind. In nearly all combinations, in the presence of heterospecific females, fewer males flew upwind and contacted or courted the source than when only conspecific females were used in the same spatial arrangement. Males did not initiate upwind flight to solely heterospecific female arrangements. Our results show that the naturally emitted pheromone plumes from heterospecific females of these three species can interfere with the ability of females to attract conspecific males when multiple females are in close proximity. However, the fact that some males still located their calling, conspecific females attests to the ability of these male moths to discriminate point source odors by processing the conflicting information from interleaved strands of attractive and antagonistic odor filaments on a split-second basis.

Heterospecific mating and partial prezygotic reproductive isolation in the planktonic marine copepods Centropages typicus and Centropages hamatus

Using three‐dimensional (3D) video observations in laboratory experiments, I describe interspecific and intergeneric mating behaviors and motility patterns of the common planktonic marine copepods Centropages typicus, Centropages hamatus, and Temora longicornis. These observations are then used to estimate heterospecific and conspecific male mate‐search volume rates and mate encounter rates in North Sea Centropages populations. Behavioral prezygotic reproductive isolation between Centropages species is incomplete, since males of each species pursued, contacted, captured, and, in rare cases, placed a spermatophore on the urosome of heterospecific females. T. longicornis males also detected the diffusible pheromone trail and pursued C. typicus females to the point of mate contact. Male mate‐search tracking behavior was equally effective on diffusible pheromone trails of heterospecific and conspecific females, indicating that pheromone and hydromechanical precontact mating cues lack species specificity. Males attempted mating with both heterospecific and conspecific females at high frequencies in the laboratory, and species recognition is inferred to occur through contact chemosensory cues or morphological incompatibility between species. Heterospecific mate encounter rates in the North Sea were maximal in late summer (August), up to~2,000 encounters m−3 d−1, and were comparable in magnitude to conspecific encounter rates during the same period. C. typicus females experience the highest incidence of heterospecific mating interactions, since they encounter heterospecific males at rates up to 100+ encounters female−1 d−1, ca. one order of magnitude higher than encounter rates with conspecifics. Heterospecific mating attempts may be a common feature of the reproductive ecology of planktonic copepods and may incur substantial fitness costs to the individuals involved.

Non-repeatable mate choice by male sailfin mollies, Poecilia latipinna, in a unisexual-bisexual mating complex

Most studies of repeatability examine female mate choice, but male mate choice may have significant evolutionary consequences when males of a sexual species are sexually parasitized by heterospecific gynogenetic females as is the case for sailfin mollies, Poecilia latipinna. Amazon mollies, Poecilia formosa, are all female gynogens that require sperm from P. latipinna for initiation of embryogenesis, but inheritance is strictly maternal. We examined repeatability and consistency of male mate choice for female sailfin versus Amazon mollies in a series of 4 experiments. We measured male association preference for 1) size-matched female sailfin versus Amazon mollies, 2) smaller female sailfin mollies versus larger Amazon mollies, and 3) larger female sailfin mollies versus smaller Amazon mollies. We also examined 4) actual male mate choice for size-matched sailfin versus Amazon mollies. Male mate preference was not repeatable in any of our studies, and male sailfin mollies were consistent in their mate preference for conspecific females over heterospecific females only when the conspecific female was larger than the Amazon and when males could actually mate with females of both species. In all experiments, males that showed the highest conspecific preference also showed the most consistency in their preference across the 2 days of testing. The lack of repeatability of male mate preference may contribute to the persistence of Amazon mollies.

Geographic variation in female mate-copying in the species complex of a unisexual fish, Poecilia formosa

Summary The Amazon molly, Poecilia formosa, is a gynogenetic, all-female fish. Its mating system relies on heterospecific matings with males of closely related sexual species. In mixed populations, males mate with conspecific sexual females and heterospecific asexual females. Such matings are not isolated dyadic interactions but rather elements of a communication network, because multiple females can observe these interactions. This is the only known case of heterospecific mate-copying and, thus, a system in which the potential for mate-copying could be influenced by the presence of another species. Here we show that mate-copying is exhibited by the sexual species P. mexicana and P. latipinna, and the asexual P. formosa . Both sexual and asexual females copy each other’s mate choice decisions in sympatry, but females from allopatric populations do not show heterospecific mate-copying. Males benefit from heterospecific matings with Amazon mollies because these increase their attractiveness to the conspecific sexual females. In mixed shoals, mate-copying potentially imposes costs as it increases a male’s attractiveness to heterospecific females. We argue that the net-effect of mate-copying is beneficial to males because the relative strength of mate-copying is lower in Amazon mollies. We hypothesize that an added benefit to males lies in the signal value of copulations.

Female mate choice determines reproductive isolation between sympatric butterflies

Animal courtship rituals are important for species recognition, and a variety of cues might be utilized to recognize conspecific mates. In this paper, we investigate different species-recognition mechanisms between two sympatric butterfly sister species: the wood white (Leptidea sinapis) and Real’s wood white (Leptidea reali). We show that males of both species frequently court heterospecific females both under laboratory and field conditions. The long-lasting elaborate courtships impose energetic costs, since the second courtship of males that were introduced to two subsequent conspecific females lasted on average only one fourth as long as the first courtship. In this paper, we demonstrate that premating reproductive isolation is dependent on female unwillingness to accept heterospecific mates. We studied female and male courtship behavior, chemical signaling, and the morphology of the sexually dimorphic antennae, one of the few male traits visible for females during courtship. We found no differences in ultraviolet (UV) reflectance and only small differences in longer wavelengths and brightness, significant between-species differences, but strongly overlapping distributions of male L. sinapis and L. reali antennal morphology and chemical signals and minor differences in courtship behavior. The lack of clear-cut between-species differences further explains the lack of male species recognition, and the overall similarity might have caused the long-lasting elaborate courtships, if females need prolonged male courtships to distinguish between con- and heterospecific suitors.

Hybridization in Calopteryx damselflies: the role of males

Females are often considered responsible for hybridization between two species because usually they are the choosier sex and their cooperation is needed for successful copulation. However, males can also be responsible for hybridization, for example in species in which males are able to force copulation. We studied the pattern of hybridization in two congeneric damselfly species, Calopteryx splendens and Calopteryx virgo, and provide evidence that F1 hybrids between the two damselfly species occur in the wild. According to mitochondrial DNA analysis, hybridization is reciprocal: five of seven hybrids were sired by C. splendens and two by C. virgo males. We conducted an experiment that revealed that males of both species have surprisingly poor premating reproductive isolation in that they accept heterospecific females, but C. splendens males were less discriminating against con- and heterospecific females than were C. virgo males. Moreover, our data on the number of hybrids sired by either species in the wild are congruent with the results of the discrimination experiment, supporting the conclusion that males may be responsible for the hybridization. Our results suggest that the males' role in hybridization studies should no longer be neglected.

Differential sperm expenditure by male sailfin mollies, Poecilia latipinna, in a unisexual–bisexual species complex and the influence of spermiation during mating

Selection should favor strategies that reduce costs associated with spermatogenesis. This is especially true when males are sympatric with closely related species, and must avoid heterospecific matings, as in the unisexual–bisexual species complex of mollies. Male sailfin mollies, Poecilia latipinna, are sexually parasitized by Amazon mollies (P. formosa), and produce more sperm in the presence of female sailfin mollies than in the presence of Amazon mollies. We tested the hypothesis that male sailfin mollies differentially expend sperm when mating with either conspecific or heterospecific females. We measured sperm expenditure by determining the amount of sperm males have remaining after mating. Male sailfin mollies had more sperm available after mating with female sailfin mollies than after mating with Amazon mollies. While this result could indicate higher sperm expenditure to Amazon mollies, males mating with female sailfin mollies had more sperm available after mating than their baseline sperm reserves. Spermiation, the last stage of spermatogenesis, could be triggered by physical contact with females, and could increase sperm availability during mating. We examined the relationship between sperm availability and the amount of time that males mated with females. We found that sperm availability increased as mating trial time increased with female sailfin mollies, but not with Amazon mollies. Spermiation in the presence of conspecific female stimuli could reduce physiological costs associated with spermatogenesis while increasing the amount and quality of sperm available for sperm competition. We suggest that future studies examining sperm priming and expenditure should consider the potential for spermiation.

Unilateral Mate Choice Causes Bilateral Behavioral Isolation Between Two Closely Related Phytophagous Ladybird Beetles (Coleoptera: Coccinellidae: Epilachninae)

AbstractBehavioral isolation between two sympatric and closely related phytophagous ladybird beetles, Henosepilachna vigintioctomaculata and Henosepilachana pustulosa, was studied in laboratory. Mating behavior was investigated using the male‐choice test. Males of H. vigintioctomaculata preferred conspecific females to heterospecific females as mates, whereas males of H. pustulosa did not show such preference. Females of H. vigintioctomaculata appeared more fastidious at mating than females of H. pustulosa, irrespective of the species of males. Males of neither species showed tenaciousness following rejection by females. The choice of conspecifics by H. vigintioctomaculata males and a difference in the intensity of rejection between H. vigintioctomaculata females (strong) and H. pustulosa females (weak) result in positive behavioral isolation in both directions of heterospecific matings. Our results thus indicated that positive unilateral mate choice yields bilateral behavioral isolation between these two species.

Sympatry with the devil: reproductive interference could hamper species coexistence

1. As species are often considered discrete natural units, interspecific sexual interactions are often disregarded as potential factors determining community composition. Nevertheless reproductive interference, ranging from signal jamming to hybridization, can have significant costs for species sharing similar signal channels. 2. We combined laboratory and field experiments to test whether the coexistence of two congeneric ground-hopper species with overlapping ranges might be influenced by sexual interactions. 3. In the laboratory experiment the number of conspecific copulations of Tetrix ceperoi decreased substantially in the presence of Tetrix subulata. Males of T. ceperoi performed more mating attempts with heterospecific females, whereas females of T. subulata rejected these heterospecific approaches more often than those of conspecifics. Although no heterospecific matings occurred in the laboratory, the reproductive success of T. ceperoi was reduced substantially in field experiments. Negative effects on T. subulata were found only at high densities. 4. Our results suggest that reproductive interference could have similar consequences as competition, such as demographic displacement of one species ('sexual exclusion'). As reproductive interference should be selected against, it may also drive the evolution of signals (reproductive character displacement) or promote habitat, spatial or temporal segregation.

Hang on or run? Copepod mating versus predation risk in contrasting environments

Mating durations of copepods were found to differ significantly between fishless high-altitude waters and lowland lakes containing fish. In lowland species the whole mating process was completed within a few minutes, but it averaged over an hour in high-altitude species. Alpine copepods showed a prolonged post-copulatory association between mates, during which the male clasped the female for an extended period after spermatophore transfer, while in lowland species males abandoned their partner immediately after copulation. Prolonged associations also occurred after transfer of spermatophores to heterospecific females with shorter conspecific mating duration, suggesting that male interests largely dictate the time spent in tandem. The differences observed may be adaptations to environments with different predation pressure, as pairs in tandem are more conspicuous and less reactive than single animals. We argue that differences in mating behavior and mating duration evolved under sexual versus natural selection, reflecting trade-offs between enhancement of fertilization success and reduction of vulnerability to visual predation. In fishless mountain lakes with high intrasexual competition, guarding males can reduce the risk of spermatophore displacement or the risk that the female will accept sperm from rival males without increased risk of being eaten, thereby maximizing paternity. Populations from fishless alpine lakes further differed from lowland species by exhibiting higher female/male size dimorphism and more intense pigmentation. While these traits vary between populations according to predation pressure, mating duration appears to be more species-specific.

Reproductive interference, priority effects and the maintenance of parapatry inSkistodiaptomuscopepods

Reproductive interactions among species, such as attempts to mate with heterospecifics, can have profound impacts on patterns of geographic range and co‐occurrence. For example, several theoretical models demonstrate that reproductive interference‐the negative influence of heterospecifics on the abilities of conspecifics to successfully mate‐can lead to parapatry, even across homogeneous landscapes, when the parapatric species are initially allopatric. However, the potential consequences of reproductive interactions on patterns of range limits and co‐occurrence have been largely ignored by ecologists. Here, I use a combination of laboratory mating experiments and a genetic survey for two parapatric species ofSkistodiaptomuscopepods to evaluate the potential importance of interspecific reproductive interactions on the maintenance of parapatry. The genetic survey demonstrates phylogenetic exclusivity of these species, suggesting that gene flow has not occurred between them. Moreover, laboratory crosses between both species demonstrate that their parapatric boundary is not maintained as a hybrid zone because the two species cannot form viable hybrids. However,Skistodiaptomus oregonensisandS. pygmaeusmales mate indiscriminately and interfere with the ability of heterospecific females to successfully reproduce. I suggest that reproductive interference results in priority effects that strongly influence the maintenance of this parapatric boundary and stress that reproductive traits are important and often‐overlooked in ecological models for species range limits.

Cross-modality effects during male–male interactions of jumping spiders

An important prediction from game theory is that the value of a resource influences the level to which male-male conflict escalates. Earlier experimental studies have shown that the seven salticid species we study here (Bavia aericeps, Euryattus sp., Hypoblemum albovittatum, Jacksonoides queenslandicus, Marpissa marina, Portia africana and Simaetha paetula) determine by sight whether a female is a conspecific or a heterospecific and then escalate the intensity with which they interact (i.e., they adopt behaviour that is likely to put them at greater risk of injury after detecting the presence of a conspecific female). Here the earlier studies are extended by using the odour of conspecific females (experimental tests) and heterospecific females (control tests), and by presenting each male with his mirror image as well as having two males interact with each other. Findings from this study suggest that, for J. queenslandicus and P. africana, the odour of conspecific females, more than the odour of heterospecific females, primes the male to escalate conflict with a potential rival. However, this was not found for the other five species tested.

Reproductive interference between Nehalennia damselfly species

We tested the hypotheses that reproductive interference between 2 congeneric damselfly species influences their local population densities and the female morph ratios in one of the species. Nehalennia irene has 2 female types (andromorph and gynomorph), whereas N. gracilis exhibits only one female type. Andromorphic N. irene females not only resemble conspecific males in body coloration, but also resemble heterospecific females of N. gracilis. We predicted male N. irene to be most attracted to gynomorphs of N. irene and male N. gracilis to be least attracted to them. Further, if N. gracilis males harass andromorphic N. irene females excessively, then they may reduce andromorph frequencies of N. irene locally. Our results indicate hybridization to be prevented by a “lock-and-key” mechanism, but male N. irene often attempt mating with female N. gracilis. Contrary to prediction, andromorph frequency in N. irene did not depend on whether N. irene populations were in sympatry or allopatry with N. gracilis. As predicted, N. irene males attempted tandem formation most frequently with conspecific gynomorphs, while N. gracilis males made most heterospecific tandem attempts on N. irene andromorphs. Collectively, our results suggest that N. gracilis females may be frequently harassed by N. irene males, and that this may help explain the relative rarity of N. gracilis.

The Role of Cuticular Hydrocarbons in Mating and Conspecific Recognition in the Closely Related Longicorn Beetles Pidonia grallatrix and P. takechii

The role of cuticular chemicals in mating behavior and their chemical components were studied in two sympatric flower-visiting longicorn beetles, Pidonia grallatrix and P. takechii. Mating experiments revealed that female cuticular chemicals elicit male mating behavior and that males can discriminate between conspecific and heterospecific females on the basis of contact chemicals. GC-MS analyses of whole-body extracts in the two species and both sexes determined that extracts contained a series of hydrocarbons including n-alkanes, n-alkenes, and methylalkanes. The relative abundance of some hydrocarbons differed between species and sexes, and canonical discriminant analysis showed discrimination of species and sex could be made unambiguously with several compounds. These results imply that the difference in cuticular hydrocarbons facilitates the premating isolation of sympatric Pidonia species.

Female choice for large body size in the cave molly, Poecilia mexicana (Poeciliidae, Teleostei): influence of species- and sex-specific cues

AbstractPrevious studies revealed that females of a cave form of the livebearing fish Poecilia mexicana (cave molly) have maintained the ancestral visual preference for large males, but — as an adaptation to life in darkness — they have evolved the novel capability to assess male size non-visually. Here we examined the mechanisms by which non-visual mate choice for large body size occurs. Are sex- and species-specific chemical cues involved in this preference for large conspecifics? We gave focal females an opportunity to associate with a large and a small stimulus fish in simultaneous choice tests, whereby the females could perceive either multiple cues (visual plus non-visual) from the stimulus fish, solely non-visual cues in darkness, or solely visual cues. Stimulus fish were two conspecific males, conspecific females, or heterospecific females (Xiphophorus hellerii). Cave molly females showed a significant preference for large conspecific males and for large conspecific females in all treatments. When a large and a small swordtail female were presented, cave molly females showed a preference for the larger fish only when exclusively visual cues from the stimulus fish were available. The non-visual preference for large body size appears to be mediated by species- but not by sex-specific cues, suggesting that species-specific chemical cues play an important role during mate choice.