Alien Males Research Articles

Studies on Mating Preference and Productivity in Drosophila ananassae and D. pallidosa and Their Hybrids

During speciation different kinds of reproductive barriers originate to preclude gene flow between diverging populations. Reproductive isolation or barriers to gene flow can be categorized by the temporal nature of their effect: pre-zygotic barriers occur before fertilization and post-zygotic barriers occur after fertilization. In this study, we studied each components of reproductive isolation between D. ananassae and D. pallidosa, including both pre-zygotic and post-zygotic barriers. Because it might be possible that by dissecting these barriers one can get the answers of many unresolved questions related to the process of speciation of these two sibling species. We reported premating isolation because females of both D. ananassae and D. pallidosa were more discriminative for mating against the alien males rather than conspecific males, and this discrimination was much stronger in case of D. ananassae females for being the ancestral and cosmopolitan species. We also did not find any decrease in the production of progeny or viable offspring in comparison to conspecific males, indicating a lack of postmating prezygotic isolating barriers. Further, there is no complete lack of intrinsic post-zygotic isolation between these species or not complete presence of post-zygotic isolation, as both the hybrid sons were producing less number of progeny in comparison to all the crosses but it is near to significant but not significant and this is contrasting to the results of a previous study.

Spider mite mothers adjust reproduction and sons' alternative reproductive tactics to immigrating alien conspecifics.

Maternal effects on environmentally induced alternative reproductive tactics (ARTs) are poorly understood but likely to be selected for if mothers can reliably predict offspring environments. We assessed maternal effects in two populations (Y and G) of herbivorous arrhenotokous spider mites Tetranychus urticae, where males conditionally express fighting and sneaking tactics in male–male combat and pre-copulatory guarding behaviour. We hypothesized that resident mothers should adjust their reproduction and sons’ ARTs to immigrating alien conspecifics in dependence of alien conspecifics posing a fitness threat or advantage. To induce maternal effects, females were exposed to own or alien socio-environments and mated to own or alien males. Across maternal and sons' reproductive traits, the maternal socio-environment induced stronger effects than the maternal mate, and G-mothers responded more strongly to Y-influence than vice versa. G-socio-environments and Y-mates enhanced maternal egg production in both populations. Maternal exposure to G-socio-environments demoted, yet maternal Y-mates promoted, guarding occurrence and timing by sons. Sneakers guarded earlier than fighters in Y-environments, whereas the opposite happened in G-environments. The endosymbiont Cardinium, present in G, did not exert any classical effect but may have played a role via the shared plant. Our study highlights interpopulation variation in immediate and anticipatory maternal responses to immigrants.

Workers select mates for queens: a possible mechanism of gene flow restriction between supercolonies of the invasive Argentine ant

Some invasive ants form large networks of mutually non-aggressive nests, i.e., supercolonies. The Argentine ant Linepithema humile forms much larger supercolonies in introduced ranges than in its native range. In both cases, it has been shown that little gene flow occurs between supercolonies of this species, though the mechanism of gene flow restriction is unknown. In this species, queens do not undertake nuptial flight, and males have to travel to foreign nests and cope with workers before gaining access to alien queens. In this study, we hypothesized that male Argentine ants receive interference from workers of alien supercolonies. To test this hypothesis, we conducted behavioral and chemical experiments using ants from two supercolonies in Japan. Workers attacked males from alien supercolonies but not those from their own supercolonies. The level of aggression against alien males was similar to that against alien workers. The frequency of severe aggression against alien males increased as the number of recipient workers increased. Cuticular hydrocarbon profiles, which serve as cues for nestmate recognition, of workers and males from the same supercolony were very similar. Workers are likely to distinguish alien males from males of their own supercolony using the profiles. It is predicted that males are subject to considerable aggression from workers when they intrude into the nests of alien supercolonies. This may be a mechanism underlying the restricted gene flow between supercolonies of Argentine ants. The Argentine ant may possess a distinctive reproductive system, where workers participate in selecting mates for their queens. We argue that the aggression of workers against alien males is a novel form of reproductive interference.

Genetic structure and reproductive strategy of the ant Cardiocondyla elegans: strictly monogynous nests invaded by unrelated sexuals

Cardiocondyla elegans is a Mediterranean ant that nests on river banks. It rears only wingless (ergatoid) males that live peacefully in the same nest as opposed to other species of the same genus, which have both peaceful, winged and mutually aggressive 'ergatoid' males. Using microsatellite analysis, we investigated the genetic structure of 21 colonies from three different locations as well as the parentage of sexuals of two colonies of C. elegans. We show that C. elegans is strictly monogynous, and that its nests can contain foreign sexuals. The presence of alien sexuals inside ant nests is described for the first time and probably counteracts inbreeding resulting from matings between siblings. In the laboratory, aggression tests showed that workers only allow alien males to enter their nests, while all winged female sexuals attempting to enter were attacked. Nevertheless, the presence of alien female sexuals in nests in the field seems to result from active carrying behaviour by workers during the reproductive period.

Sex Differences in Territorial Behavior Exhibited by the Spotted Hyena (Hyaenidae, Crocuta crocuta)

Spotted hyenas (Crocuta crocuta) are gregarious carnivores that defend group territories against encroachment by neighboring conspecifics. Here we monitored the behavior of members of one clan of free‐ranging spotted hyenas during border patrols, ‘wars’ with neighboring clans, and other interactions with alien intruders, to document differences between the sexes in territorial behavior in this species. We also examined the possibility that the probability or rate of attack on alien hyenas encountered within the clan’s territory would vary with the sex of the intruders. Initiation and leadership of most cooperative territorial behaviors were by adult female clan members, although border patrols were occasionally conducted by groups composed exclusively of resident males. The vast majority of alien intruders into the territory of the study clan were males. Resident females were more likely to attack intruding females than intruding males, but hourly rates of aggression directed by females towards aliens did not vary with intruder sex. Resident males were more likely than resident females to attack alien males, and resident males directed significantly higher hourly rates of aggression towards intruding males than females. Although female leadership in most cooperative territorial behaviors distinguishes spotted hyenas from many mammalian carnivores, other sex differences in the territorial behavior of spotted hyenas resemble those documented in other gregarious predators. Sex differences observed in hyena territoriality are consistent with the hypothesis that male and female clan members derive different selective benefits from advertisement and defense of group territories.

Effects of physiological and social challenges in different seasons on fecal testosterone and corticosterone in male domestic geese ( Anser domesticus )

We investigated the reliability of the non-invasive approach of measuring steroid hormones from feces in the domestic goose (Anser domesticus), a mainly herbivorous bird with a short gut passage time (2–3 h). Groups of eight outdoor-housed male domestic geese were subjected to three different experiments, injection of either GnRH analogue or ACTH, or ”social stimulation” by confrontation with two alien males or females. These experiments were replicated in three different seasons, in spring, during peak reproductive activity, in summer, during long-day photorefractoriness and postnuptial molt, and in fall, during sexual reactivation. GnRH stimulation resulted in significant increases of mean response and peak fecal testosterone metabolites (TM) in spring and fall. Response TM concentrations excreted in spring were generally higher than in summer and fall. Social confrontation with two females, but not with two males, increased mean and peak TM in all seasons. In general, ACTH treatment resulted in a proportionally higher increase of fecal corticosterone metabolites (BM) than GnRH did in fecal TM (80- to 140-fold vs 6- to 8-fold). ACTH significantly increased mean and peak BM in all seasons. Social confrontation with two males significantly increased fecal BM in spring, but confrontation with two females increased fecal BM in fall. Our results indicate that determining steroids from feces is a generally valid approach. However, the sensitivity of the method may vary between different hormones and results may differ between seasons. BM results seemed more sensitive and seasonally robust than did TM.

Social wasp swarm emigration: males stay behind

Many species of tropical social wasps initiate colonies by means of a swarm of queens and workers. Swarms either bud from mature colonies (reproductive swarms) or form from the entire adult population when it evacuates following destruction of the nest by predation or accident (absconding swarms). Colonies giving rise to founding swarms of either type may have males in their populations. Swarms emigrate along a chemical trail to a site selected by scouts, where the workers begin building a new nest. Published analyses of newly-founded colonies indicate that such colonies occasionally contain males. This raises the question of whether these are alien males who joined the new colony shortly after its founding, or are siblings of the females, having emigrated with them from the natal nest site. We used a double censusing technique to determine whether males of the Neotropical social wasp, Polybia occidentalis, emigrate with females in absconding swarms. Nine absconding swarms in Costa Rica were censused and sexed directly before they emigrated and were shown to contain males as well as females. When the swarms departed for the new site, males remained behind, and when the swarms were censused again soon after reaching their new sites, none contained males. Thus males of this species cluster temporarily with absconding females, but fail to emigrate with them. We suggest that the males’ failure to join pre-emergence colonies is in the best interest of both sexes.

Embryonic abnormality caused by male pheromonal effect in pregnancy block in mice.

BALB/cA females mated with BALB/cA males and exposed to DDK males showed 100% pregnancy block when exposure started at Days 0-3 of pregnancy. When the exposure to DDK males started at Days 4, 5, 6, and 7, the pregnancy rate was 33.3%, 50%, 90%, and 100%, respectively. (Hereafter, the BALB/cA females exposed to DDK males are referred to as the experimental females, and those exposed to other BALB/cA males as the control females.) Cell number of embryos at Day 3 of pregnancy from the experimental and control females after exposure starting from Day 0 was, respectively, 27.0 +/- 1.2 (mean +/- SEM) vs. 48.6 +/- 1.0 (p < 0.05) for the morulae and 34.8 +/- 1.3 vs. 64.1 +/- 2.0 (p < 0.05) for the blastocysts. Embryos from the experimental and control females after exposure starting from Day 3 or Day 4 were histologically examined after 24-h exposure. Poor development of trophoblast and inner cell mass was observed at Day 4 as general defects of the experimental embryos. In addition, about one third of the embryos were unexpectedly at the more advanced stages than the controls (abnormal overdevelopment). At Day 5, disintegration of the trophoblast layer and primitive endoderm was observed as common abnormalities of experimental embryos, but overdevelopment was not observed at this stage. Disturbance in trophoblast differentiation or failure of its maintenance may be the primary developmental defect displayed by embryos developing in a deteriorated uterine environment under the influence of the odor of alien males.

Effect of cyproterone acetate on the pregnancy-blocking ability of male mice and the possible chemical nature of the pheromone.

Even though castration abolished the ability of alien males to induce implantation failure (the Bruce effect) in newly inseminated females, treatment of intact alien males with the steroidal antiandrogen, cyproterone acetate, for 14 days (short term) did not significantly depress their ability to induce the Bruce effect. However, prolonged treatment (42 days) with cyproterone acetate suppressed the pregnancy-blocking ability of alien males to some extent, possibly due to the antigonadotrophic properties of the drug. Ovariectomized alien females treated with implants of testosterone (androgenized females) exhibited the ability to block implantation in newly inseminated females, but concurrent treatment of androgenized females with cyproterone acetate did not depress this ability. The results strongly suggest that the pheromone involved in the male-induced implantation failure is not the product of an androgen-dependent tissue, but is likely to be a product of androgen metabolism.

Induction of pseudopregnancy in pregnancy-blocked mice by re-exposure to stud males

Re-exposure to stud males beginning on day 4 post coitum induced pseudopregnancy in a large proportion of female mice whose pregnancies were terminated by a single injection of 0.5 mg of bromocriptine on day 1 post coitum. By contrast, exposure to alien or strange males was ineffective in inducing pseudo-pregnancy in pregnancy-blocked females. The results suggest that the newly inseminated female retains the memory of the stud male for some days after mating. Activation of the ‘memory’ by pheromones of the stud males exerts a luteotrophic effect in pregnancy-blocked females resulting in the incidence of pseudopregnancy. This may account for the inability of the stud male to block pregnancy in his coital partner and also for the inability of alien males to block implantation in newly inseminated females housed with stud males.

Chemosensory recognition of mouse major histocompatibility types by another species.

Mice can recognize one another by individually characteristic body scents that reflect their genetic constitution at the extremely polymorphic major histocompatibility complex (MHC) of genes on chromosome 17. Reproductive behavioral manifestations of this sensory communication system include MHC-related mating preferences and neuroendocrine responses that affect preimplantation pregnancy and arise from the MHC-related scent of alien males. We have shown previously that mice can be trained in a Y maze to distinguish the scents of urine of congeneic mice that differ genetically only at the MHC. By means of an automated olfactometer, we now show that rats also can similarly distinguish the urinary scents of MHC congeneic mice. Thus, the mode of individual recognition that depends on scents determined by MHC genes can operate across species barriers.

Studies of the male-originating pheromones involved in the Whitten effect and Bruce effect in mice.

Experiments were designed to elucidate the mode of transmission of the male-originating pheromones involved in the induction of estrus (the Whitten effect) and in implantation failure (the Bruce effect) in mice. The Whitten effect was induced in unisexually grouped females by exposure to corralled males, and also by corralled males housed within a perforated cage (which prevented physical contact of the females with the male-originating pheromone). The results suggest that the pheromone involved in the Whitten effect is volatile (airborne). Implantation failure occurred in a significantly high proportion of newly inseminated females when they were individually confined in corrals and housed below corralled alien males. By contrast, implantation failure was significantly reduced when corralled females were housed above corralled alien males. The results indicate that the male-originating pheromone involved in the Bruce effect is nonvolatile and acts on the females through contact. It is suggested that the pheromone involved in the Whitten effect is distinct from the one involved in the Bruce effect.

Involvement of contact stimuli in the male-induced implantation block (the Bruce effect) in mice

Confinement of newly inseminated female mice exposed to confined alien males significantly decreased the male-induced implantation failure (the Bruce effect). By contrast, free (unconfined) females exposed to confined alien males showed a high rate of implantation failure. The results suggest that the pheromone of male origin involved in the Bruce effect is non-volatile and acts on the female through contact. The vomeronasal organ appears to be involved in the perception of this pheromone.

The antennae and mating behaviour ofDrosophila females

The females ofDrosophila bipectinata andD. malerkotliana are able to discriminate between their own and alien males in the absence of antennae. Thus mate recognition seems to depend on contact chemoreceptors in these 2 species.

Studies on the pheromonal pregnancy block in the mice. I. Strain differences of mice in pheromonal pregnancy block (author's transl)

Strain differences of mice in the "Bruce effect" were examined among five inbred strains ; C3H, C57BL/6, BALB/c, CBA and DDY. For mating, 3 virgin adult females were caged together with an adult male at 8 approximately 20 weeks of age, and checked daily for copulation for a maximum of 10 days. The females were removed from the male when the vaginal plug was found, and housed with strange or alien males for 8 or 15 days. The "Bruce effect" was evident in C3H, BALB/c, CBA and DDY strains having high percentages of blocked pregnancies on alien males. In contrast, C57BL/6 strain showed no such effect. Based on these findings, it was concluded that "Bruce effect" caused by alien male pheromone showed strain differences among different strains of mice.

Response of a Cotton Rat Population to Increased Density

Experiments were conducted in old-field enclosures to define some of the responses of a confined, nonreproducing cotton rat population to increases in density. Successive groups of alien animals were randomly added to a monitored resident population on two occasions. Aliens exhibited high rates of mortality and weight loss. The alien males were particularly affected, only 18 percent surviving the experiment. Residents could not be accounted for by trapping as easily as aliens. Residents concentrated in discrete areas of preferred habitat yet ranged over the entire enclosure, while aliens stayed in heavy ground cover close to the walls. Analysis of the average distance between captures of each group on a daily basis revealed increases in resident movements and corresponding decreases in alien movements. Changes in spatial distribution, movement patterns, sex ratio and rats of mortality due to trap deaths and predation in the alien groups reflected behavioral interactions that operate as a form of social exclusion.

Effects of social rank and social disruption in adult male house mice

In agreement with previous work, adrenocortical activity was increased and survival reduced among subordinate male mice. Adrenocortical activity was increased further and survival lowered among those subordinates which were moved daily for 7 days into a strange physical and social environment. Increased activity of the adrenal cortex was indicated in dominant animals and was independent of social disruption due to repeated introduction of alien males. Renal glomerular lesions and inhibited secretion of androgens were apparent only in subordinate individuals.

Olfactory pregnancy-block in mice ( Mus musculus): An unusual response acquisition paradigm

Females of the Parkes strain ( Mus musculus) were bred during either a short-term (3 hr) or long-term (24 hr or more) exposure to Parkes strain studs. After breeding they were exposed to the urine of CBA males. The short-term females had significantly higher fertility (63 per cent) than long-term females (34 per cent). This supports the hypothesis that the effect of exposure to the stud male during breeding is to ‘sensitize’ the female to stimulation by the alien males. Re-exposing short-term females to their stud males did not affect their pregnancy rate nor did the short period of exposure to the stud male result in a lower fertility rate.

Pregnancy-block in female mice placed in boxes soiled by males.

Summary. Newly mated female mice were placed singly for periods of up to 3 days in boxes recently vacated by five males of a different strain (alien males). When the soiled boxes were renewed twice daily, the females showed pregnancy-block to the same extent as when placed in the proximity of alien males for similar periods. When the soiled boxes were renewed once daily, the incidence of pregnancy-block was much reduced. An equal amount of disturbance, caused by similarly transferring the females to clean cages, did not affect the incidence of pregnancy. These results support previous work in indicating that the smell of the alien male is the operative factor in pregnancy-block, and further suggest that the odorous substances involved are highly evanescent.