Interspecific Copulation Research Articles

First Records of Picobiine Mites Associated with Birds-of-Paradise: Can Interspecific Sexual Behaviour of Hosts Play a Role in the Distribution of Quill Mite Parasites?

While birds-of-paradise (Passeriformes: Paradisaeidae) are a well-known group of birds, our understanding of their parasites is still limited. This study reports on parasitic quill mites of the subfamily Picobiinae (Acariformes: Syringophilidae), which have never before been recorded on this group of birds. The mite specimens presented in this paper were collected from birds-of-paradise that had been captured in Papua New Guinea and Indonesia in the years 1910-1911 and are now deposited in the Bavarian State Collection of Zoology, Munich, Germany. Two syringophilid species are described as new to science: (i) Picobia frankei sp. n. from the magnificent riflebird Lophorina magnifica, the glossy-mantled manucode Manucodia ater, and the crinkle-collared manucode Manucodia chalybatus, and (ii) Gunabopicobia garylarsoni sp. n. from the twelve-wired bird-of-paradise Seleucidis melanoleucus and the lesser bird-of-paradise Paradisaea minor. We hypothesise that the presence of both picobiine species on phylogenetically unrelated paradisaeids may be caused by the sexual behaviour of these birds, where interspecific copulations may play a role in the switching of parasites between non-closely related host species.

Interspecific forced copulations generate most hybrids in broadly sympatric ducks

Although rare, hybrids are more common in broadly sympatric waterfowl than in any other avian family; yet, the behavioral ecology explaining their generation has remained controversial. Leading hypotheses are forced interspecific copulations, mis-imprinting caused by mixed broods, and scarcity of conspecific mates. Using a large sample of hybrid ducks solicited from North American hunters we evaluated these hypotheses by genetically determining the mother and father species of F1 hybrids. Based on abundances in areas where their breeding ranges overlap, the frequency of hybrids varied greatly from expectations, with hybrids between species within recently derived clades being much more frequent than those between more divergent clades. Forced copulations, as measured by large phallus-length asymmetries between parentals, strongly predicted the father species of most F1 hybrids. Thus, most Anas acuta x A. platyrhynchos (Northern Pintail x Mallard) F1s were sired by A. acuta, and most A. platyrhynchos x Mareca strepera (Mallard x Gadwall) F1s were sired by A. platyrhynchos. Siring asymmetries were consistent with phallus length asymmetries in five additional parental combinations, but none had samples large enough to be individually statistically significant. The exception to this trend was our sample of nine A. platyrhynchos x Mareca americana (Mallard x Gadwall) F1s, for which a large phallus asymmetry failed to predict the father species. Hybrids were rare in brood parasitic species, suggesting mis-imprinting to be an unlikely cause of most hybrids; however, our samples of hybrids from regular brood parasites were inadequate to strongly address this hypothesis. We could test the scarcity of mates hypothesis for only a single hybrid combination and it contradicted our prediction: most F1 M. Penelope x M. americana (Eurasian x American Wigeon) were sired by M. penelope, strongly contradicting our prediction that female M. penelope wintering in enormous flocks of M. americana (American Wigeon) on the west coast of North America would have difficulty finding conspecific mates. In general, our results support interspecific forced copulations as the predominant behavioral mechanism generating hybrids in North temperate waterfowl.

Insemination in Aedes aegypti and Aedes albopictus.

Aedes mosquitoes are the vectors of several arboviruses that cause human disease. A better understanding of their reproduction helps to improve their management and contributes insights into the fundamental biology of mosquitoes. During mating, inseminated mosquito females receive seminal fluids and sperm from males that they then store in the spermathecae. In Aedes aegypti and Aedes albopictus, most mated females become resistant to further insemination within 2 h of initial insemination. Although the male seminal fluids are known to be involved in initiating the resistance of inseminated females to further insemination, the mechanism underlying this resistance is not well-understood. The determination of insemination status is a key step in investigating the behavioral and molecular interactions between males and females and for exploring the proximate influences and evolutionary implications of interspecific copulations. Several methods exist for determining insemination status, as discussed here. The choice of method depends on the research question and the availability of resources.

Extraspecific copulation in Coleoptera

Interspecific, intergeneric and interfamilial copulation in Coleoptera are rarely observed and even more rarely photographed in the wild. Records are summarised and two new observations from Cyprus and England are documented and illustrated.

Previous Interspecific Courtship Impairs Female Receptivity to Conspecifics in the Parasitoid Wasp Nasonia longicornis But Not in N. vitripennis.

Interspecific sexual interactions are not uncommon in animals. In sympatry, females often face the risk of accidentally mating with a heterospecific male. Based on the actual risks imposed by the environment at a given time and place, females should be able to adjust their mate acceptance in order to avoid interspecific copulations as well as accidentally refusing to mate with a conspecific. We investigate the ability of females of the two parasitoid wasp species Nasonia vitripennis (Nv) and N. longicornis (Nl) to adjust their mate acceptance in response to previous unsuccessful courtship by heterospecific males. We show that Nl females are more reluctant to mate with a conspecific male when having been courted previously by a heterospecific male, but Nv females are not. We argue that this strategy is reasonable for Nl females but not for Nv females, which follow a different strategy to avoid the fitness costs imposed by heterospecific copulations.

A Major Locus Controls a Genital Shape Difference Involved in Reproductive Isolation Between Drosophila yakuba and Drosophila santomea.

Rapid evolution of genitalia shape, a widespread phenomenon in animals with internal fertilization, offers the opportunity to dissect the genetic architecture of morphological evolution linked to sexual selection and speciation. Most quantitative trait loci (QTL) mapping studies of genitalia divergence have focused on Drosophila melanogaster and its three most closely related species, D. simulans, D. mauritiana, and D. sechellia, and have suggested that the genetic basis of genitalia evolution involves many loci. We report the first genetic study of male genitalia evolution between D. yakuba and D. santomea, two species of the D. melanogaster species subgroup. We focus on male ventral branches, which harm females during interspecific copulation. Using landmark-based geometric morphometrics, we characterized shape variation in parental species, F1 hybrids, and backcross progeny and show that the main axis of shape variation within the backcross population matches the interspecific variation between parental species. For genotyping, we developed a new molecular method to perform multiplexed shotgun genotyping (MSG), which allowed us to prepare genomic DNA libraries from 365 backcross individuals in a few days using little DNA. We detected only three QTL, one of which spans 2.7 Mb and exhibits a highly significant effect on shape variation that can be linked to the harmfulness of the ventral branches. We conclude that the genetic architecture of genitalia morphology divergence may not always be as complex as suggested by previous studies.

What the direction of matings can tell us of hybridisation mechanisms in ducks

Interspecific hybridisation is common amongst birds and is associated with diverse costs and benefits. Several mechanisms are thought to promote hybridisation, including heterospecific mate choice, species recognition errors and interspecific forced copulations. Discriminating between these mechanisms is often problematic due to difficulties in observing interspecies copulations in the wild. The directionality of hybridisation may, however, provide some insights into which mechanisms are operating. For example, matings may be unidirectional when females prefer to mate with heterospecific males with a specific trait, such as higher dominance or a supernormal stimulus. In contrast, bidirectional hybridisation is more likely when other mechanisms, such as heterospecific imprinting as a result of brood mixing, are operating. We here characterise the direction of matings between Grey Teal (Anas gracilis) x Pacific Black Duck (A. superciliosa) hybrids. By sequencing a fragment of the maternally inherited mitochondrial DNA, we show that hybridisation occurs bidirectionally between these species. This suggests that a female preference does not exist in both species for a specific male trait of only one species. We suggest that errors in species recognition are improbable and that heterospecific mate choice, possibly due to brood mixing, may more likely promote hybridisation between Grey Teals and Pacific Black Ducks.

Exaggerated male genitalia intensify interspecific reproductive interference by damaging heterospecific female genitalia

Male-male competition over fertilization can select for harmful male genital structures that reduce the fitness of their mates, if the structures increase the male's fertilization success. During secondary contact between two allopatrically formed, closely related species, harmful male genitalia may also reduce the fitness of heterospecific females given interspecific copulation. We performed a laboratory experiment to determine whether the extent of genital spine exaggeration in Callosobruchus chinensis males affects the fitness of C. maculatus females by injuring their reproductive organs. We found that males with more exaggerated genital spines were more likely to injure the females via interspecific copulation and that the genital injury translated into fecundity loss. Thus, as predicted, reproductive interference by C. chinensis males on C. maculatus females is mediated by exaggeration of the genital spine, which is the evolutionary consequence of intraspecific male-male competition. Harmful male traits, such as genital spines, might generally affect the extent of interaction between closely related species.

Does heterospecific seminal fluid reduce fecundity in interspecific copulation between seed beetles?

Reproductive interference through mating between related species can cause fitness reduction and affect population dynamics of the interacting species. In experimental matings between two seed beetles, Callosobruchus chinensis and Callosobruchus maculatus, C. maculatus females, but not C. chinensis females, suffer from significant loss of fecundity when conspecific mating is followed by heterospecific mating. We hypothesized that male traits associated with sexual conflict, which are often harmful to females, pleiotropically affect fitness of heterospecific females through interspecific mating. We examined the effect of ejaculate of C. chinensis males on C. maculatus females as the cause of the fecundity loss in C. maculatus females due to interspecific copulation. We found that frequent interspecific copulation occurred between C. maculatus females and C. chinensis males, but not between C. chinensis females and C. maculatus males, resulting in frequent interspecific ejaculate transfer from C. chinensis males to C. maculatus females. However, injection of the extract from C. chinensis male reproductive organs into C. maculatus females did not significantly affect C. maculatus fecundity compared with saline injection, indicating that the effect of the heterospecific ejaculate transfer on fecundity is negligible. We suggest that other harmful male traits such as genital spines of C. chinensis males are mainly responsible for the fecundity reduction in C. maculatus females that have experienced interspecific mating.

Many a slip: dissecting the causes of reproductive isolation in two species ofTegenariaspiders (Agelenidae)

Key to our understanding of the mechanisms underlying the process of speciation is the determination of the nature of the barriers to gene flow between related taxa. Species that show zero gene flow in sympatry or parapatry are of little use in this respect. In the present study, we used two closely-related species of large house spider, Tegenaria saeva and Tegenaria gigantea, which hybridize to a limited extent along a natural contact zone in southern Britain. The species are apparently indistinguishable with respect to habitat utilization and phenology. Laboratory crosses using individuals from both allopatric and parapatric populations suggest that, although male and female courtship, as well as web and cuticular-borne pheromones, are conserved between the species, mechanical difficulties are experienced during interspecific copulation. Copulation bouts are, on average, significantly shorter during interspecific matings because of these difficulties, and are probably not sufficiently long for effective sperm transfer to take place. In the two cases of successful interspecific crossing, and in subsequent F1 and backcross generations, there are few indications of differential fertility, fecundity or viability, suggesting little post-zygotic incompatibility. The high success rate of crosses between F1 hybrids and both parental species underlines the principally mechanical barrier to gene flow between these taxa. Once this is breached, there appears to be little impediment to continuing introgression, which could, in some geographical areas at least, ultimately lead to the fusion of the two species. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113, 355–367.

Testing for reproductive interference in the population dynamics of two congeneric species of herbivorous mites.

When phylogenetically close, two competing species may reproductively interfere, and thereby affect their population dynamics. We tested for reproductive interference (RI) between two congeneric haplo-diploid spider mites, Tetranychus evansi and Tetranychus urticae, by investigating their interspecific mating and their population dynamics when they competed on the same plants. They are both pests of tomato, but differ in the host plant defences that they suppress or induce. To reduce the effect of plant-mediated interaction, we used a mutant tomato plant lacking jasmonate-mediated anti-herbivore defences in the competition experiment. In addition, to manipulate the effect of RI, we introduced founder females already mated with conspecific males in mild RI treatments or founder, virgin females in strong RI treatments (in either case together with heterospecific and conspecific males). As females show first-male sperm precedence, RI should occur especially in the founder generation under strong RI treatments. We found that T. urticae outcompeted T. evansi in mild, but not in strong RI treatments. Thus, T. evansi interfered reproductively with T. urticae. This result was supported by crossing experiments showing frequent interspecific copulations, strong postmating reproductive isolation and a preference of T. evansi males to mate with T. urticae (instead of conspecific) females, whereas T. urticae males preferred conspecific females. We conclude that interspecific mating comes at a cost due to asymmetric mate preferences of males. Because RI by T. evansi can improve its competitiveness to T. urticae, we propose that RI partly explains why T. evansi became invasive in Europe where T. urticae is endemic.

How the length of genital parts affects copulation performance in a carabid beetle: implications for correlated genital evolution between the sexes

To identify factors leading to the correlated evolution of exaggerated male and female genitalia, we studied the effects of the variable dimensions of corresponding functional genital parts (male copulatory piece and female vaginal appendix) on copulatory performance in the polygamous carabid beetle Carabus (Ohomopterus) maiyasanus. We used mating pairs of individuals from two populations to increase the variances in genital dimensions and determined the copulation performance (insemination and spermatophore replacement, and copulation time) in single- and double-mating situations. In single mating, insemination success was not affected by genital dimensions, although the copulation time was significantly shorter when the male aedeagus was longer. In the double-mating experiment, insemination and replacement of spermatophores by the second male succeeded more frequently when the copulatory piece was shorter and the vaginal appendix was longer, and when the difference between the length of the copulatory piece and the vaginal appendix was smaller. Thus, a matching of the corresponding genital parts between the sexes increases the male's reproductive success in sperm competition, but elongation of the copulatory piece cannot be explained simply by the improvement in male reproductive success. We discuss possible factors for the elongation of genital parts in terms of sexual conflict and reproductive interference through interspecific copulation.

Confusion and Isolation in the Courtship of Two Sympatric and Synchronic Tarantula Spiders (Mygalomorphae, Theraphosidae)

Summary Strong reproductive barriers are expected between similar species that co-occur in time and space. We experimentally analysed sexual interactions between the theraphosids Acanthoscurria suina and Eupalaestrus weijenberghi which met those conditions. Unexpectedly, males courted on heterospecific female cues. Furthermore, A. suina females seemed to be more receptive to heterospecific males than conspecific ones in early courtship. Although precopulatory confusion occurred, no interspecific copulations were observed, which indicate that reproductive barriers operate.

The mechanism of the fecundity reduction in Callosobruchus maculatus caused by Callosobruchus chinensis males

AbstractMale promiscuity sometimes results in interspecific reproductive interaction, also known as reproductive interference. Reproductive interference entails costs for the individuals involved and affects the community structure by reducing the population growth rate. However, our understanding of the mechanisms generating reproductive interference is still insufficient. Two congeneric bean weevils, Callosobruchus chinensis and C. maculatus, show asymmetric reproductive interference; only C. chinensis males reduce the fecundity of the other species. Here we investigated the mechanism of reproductive interference by C. chinensis males on C. maculatus females in terms of lifetime fecundity. Callosobruchus chinensis males with ablated genitals, which could harass C. maculatus females but not copulate with them, did not reduce the C. maculatus fecundity, suggesting that interspecific copulation was necessary. However, a single interspecific copulation did not affect C. maculatus fecundity as long as the females also copulated with a conspecific male. Exposure to C. chinensis males for 24 h prior to oviposition significantly reduced C. maculatus fecundity, and fecundity was negatively correlated with the number of C. chinensis males the females were exposed to. Additionally, C. maculatus females experienced more interspecific copulations when they were housed with more C. chinensis males. Together these findings suggest that multiple interspecific copulations by C. chinensis males reduce the fecundity of C. maculatus females. Thus in general, even if a single interspecific copulation is apparently harmless, repeated interspecific copulations can be costly for the individuals involved. Furthermore, only by quantifying reproductive success were we able to identify the precise mechanism of reproductive interference.

Sex Bias in Interspecific Copulation between the Hermaphroditic Freshwater Snails,Physa acutaandP. pomilia(Physidae)

Previously-published mate-choice experiments have uncovered significant prezygotic reproductive isolation between South Carolina populations of Physa acuta (Draparnaud, 1805) and P. pomilia (Conrad, 1834). Here we report the results of similar tests returning no evidence of such barriers between an Alabama population of P. pomilia and three separate populations of P. acuta, two from Alabama and one from South Carolina. However, heterogametic copulations did demonstrate both a significant sex bias and a significant size bias. The smaller P. acuta was more likely to copulate in the male role and hence less exposed to any potential fitness decrements due to the reduced viability and sterility of the hybrids produced. Our observations on defeated mating attempts suggested that P. acuta may be more aggressive than Alabama P. pomilia in mating contests (its smaller size perhaps contributing to greater agility) and hence more likely to prevail in the male role. The absence of a sex bias in our previously-published mate-choice observations involving South Carolina P. pomilia and P. acuta may be attributable to our use of size-matched snails, which equalized the agility of the prospective copulants, thus perhaps prolonging the mating contests, and ultimately lessening the likelihood that any mating took place at all.

Species of the genus Eurydema (Hemiptera: Heteroptera: Pentatomidae) in Far East Asia: An integrated approach using morphological, molecular, and data crossing analyses for taxonomy

In a revision of four previously described species of the genus Eurydema in Far East Asia, we confirm only two species, one of which consists of two subspecies: E. dominulus (Scopoli 1763) [= E. pulchra (Westwood 1837), syn. nov.], E. gebleri gebleri Kolenati 1846, and E. gebleri rugosa Motschulsky 1861 [stat. nov.]. In order to prove the above taxonomic changes, we focused on three major analyses; (1) morphological study (color patterns), (2) molecular identification (DNA barcording) and (3) cross–breeding (inter–specific copulation, fertilization). The results of these analyses were sufficient to confirm the new taxonomic changes. According to the cross–breeding analysis, interspecific copulation between males of E. dominulus (= E. pulchra) and females of E. g. gebleri or E. g. rugosa occurs in nature, but the eggs laid by the interspecific copulation were unfertilized. Two subspecies, E. g. rugosa and E. g. gebleri, preserve their own unique coloration patterns; this was confirmed by the results of intra–subspecific copulation and breeding. However, the 1 st progeny from the inter–subspecific copulation of E. g. rugosa♂ X E. g. gebleri♀ (or E. g. gebleri♂ X E. g. rugosa♀) were confirmed to have the coloration patterns inherited from E. g. gebleri.

A potential species-specific molecular marker suggests interspecific hybridization between sibling species Littorina arcana and L. saxatilis (Mollusca, Caenogastropoda) in natural populations

Three sister species of rough periwinkles, viz. Littorina saxatilis (Olivi 1792), L. arcana (Hannaford Ellis 1978) and L. compressa (Jeffreys 1865) from the Barents Sea (Russia), the White Sea (Russia) and the Norwegian Sea (Norway) were studied. The identification of two sibling species L. saxatilis and L. arcana is often difficult as both species have extremely similar shell morphology and reproductive systems. Only mature females can be unambiguously distinguished, with a jelly gland present in female L. arcana, but which is replaced by a brood pouch containing developing embryos in L. saxatilis. No clear-cut diagnostic features have been found to discriminate between males or juveniles of the two species. The very first diagnostic DNA marker (DNA fragment A2.8, 271 bp length) for L. arcana and L. saxatilis separation was developed. The marker was derived from apparently species-specific L. arcana DNA fragments obtained via Random Amplified Polymorphic DNA (RAPD) analysis. This fragment was cloned and sequenced, whereupon specific primers were designed and the amplification was surveyed in a large number of morphologically well-identified females of both species. Subsequently, the specific DNA marker was used for the identification of male L. arcana and partners in copulating pairs. In this way, we obtained evidence of possible interspecific hybridization between the sibling species L. arcana and L. saxatilis living in sympatry in natural populations: the presence of A2.8 fragment in 12% of morphologically well identified L. saxatilis females and its absence in 14% of morphologically well identified L. arcana females. The A2.8 fragment never amplified in L. saxatilis from sites without L. arcana. The A2.8 fragment did not amplify in L. compressa, not even in microsympatric populations, and we did not observe interspecific copulations between L. arcana and L. compressa.

Asymmetric reproductive isolation during simultaneous reciprocal mating in pulmonates

The generality of asymmetric reproductive isolation between reciprocal crosses suggests that the evolution of isolation mechanisms often proceeds in reciprocal asymmetry. In hermaphroditic snails that copulate simultaneously and reciprocally, asymmetry in premating isolation may not be readily detectable because the failure of the symmetric performance of courtship would prevent copulation from occurring. On the other hand, through their prolonged copulation, snails discriminate among mates when exchanging spermatophores for their benefit and thus may exhibit asymmetric reproductive isolation during interspecific mating. However, no clear case of reciprocal asymmetry has been found in reproductive isolation between snail species. Here we show a discrete difference in hybridization success between simultaneous reciprocal copulations between two species of pulmonate snails. Premating isolation of Bradybaena pellucida (BP) and Bradybaena similaris (BS) is incomplete in captivity. In interspecific copulation, BP removes its penis without transferring a spermatophore, while BS sires hybrids by inseminating BP. Thus, 'male' BP or 'female' BS rejects the other individual, while female BP and male BS accept each other, so that the two sexes of either BP or BS oppose each other in mate discrimination. Our results are a clear example of asymmetry in reproductive isolation during simultaneous reciprocal mating between hermaphroditic animals.

Sexual harassment of a king penguin by an Antarctic fur seal

Males of gregarious pinnipeds are often aggressive to conspecifics and sexual coercion of females is commonplace. Males of some pinniped species have been known to attempt interspecific copulation, occasionally being successful in producing hybrid offspring. The most extreme case of interspecific sexual coercion reported concerned species from different families. We report a case of interspecific sexual harassment bridging the rank of vertebrate class.

Comparative morphology and cytology of the male sperm‐transmission organs in viviparous species of clinid fishes (Clinidae: Teleostei, Perciformes)

This work comprises the first comparative study of the morphology and cytology of the sperm transmission organs in males of 14 species of viviparous clinid fishes (Clinidae, Blennioidei, Teleostei). The form and dimensions of these organs differ among the various species studied. The organs are composed of intra-abdominal ampullae, into which the sperm ducts and urinary bladder anchor, and an external protruding intromittent papilla used for insemination. The form of the ampullae differs among the various species, from pear-shaped to horseshoe-shaped. It increases in dimensions with increasing length of the male. In all the species this organ is covered by a connective-tissue tunic that encompasses both circular and longitudinal striated muscle bundles. The lumina of the ampullae harbor the epididymis, a strongly convoluted and plicated duct, which becomes filled with spermatozeugmata during reproduction. From here, the epididymis continues into the protruding intromittent papillae, where its folds gradually straighten at the apical part of the intromittent organ. The form and dimensions of this copulatory organ also differ in the various species. Papillae bearing taste buds are found on the apical parts of the intromittent organ, and it is probable that these, together with the difference in forms of the organ, help to prevent interspecific copulation.