Copulation Frequency Research Articles

Distinct behavioural strategies underlying asymmetric mating interactions between invasive and indigenous whiteflies

AbstractKnowledge of animal mating strategy may provide insight into the evolution of mating behaviour, speciation, and species competition interactions. Our previous study showed that asymmetric mating interactions between invasive and indigenous species of the worldwide distributed whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) complex contribute to invasion and displacement. Here, we reobserved in detail the video recordings of mating behaviour and behavioural interactions of a previous study and did an integrated analysis on the new data obtained here and some aspects of the data reported earlier. We compared the mating strategies of an invasive whitefly species and an indigenous congeneric competitor from each of two geographic regions, China and Australia. We found that in both regions, females of the invasive species had higher propensity to copulate than those of the indigenous species. In addition, females of the invasive species increased their frequency of copulation in response to increases in courting by males. Compared with males of the indigenous species, those of the invasive species were more likely to court per unit time as well as to interrupt courting pairs, and they also exhibited shorter durations of copulation. In addition, males of the invasive species exhibited post‐copulatory guarding behaviour, whereas those of the indigenous species did not. The different mating strategies exhibited by the invasive and indigenous species may be the evolutionary basis of their asymmetric mating interactions. Such differences in mating strategies confer on the invasive whitefly species the capacity to both invade and displace indigenous whitefly competitors.

Male mating behaviour in relation to female sexual swellings, socio-sexual behaviour and hormonal changes in wild Barbary macaques

In many cercopithecine primates females display probabilistic cues of fertility to indicate the periovulatory period to males. These cues may include female behaviour, acoustic signals, and morphological signs such as the anogenital swelling. However, the extent to which males can utilise this information varies between species. We describe male sexual behaviour in relation to changes in anogenital swelling size, timing of ovulation and female socio-sexual behaviour in wild Barbary macaques (Macaca sylvanus). We further compare male sexual behaviour during conception and post-conception cycles to evaluate if males differentiate between these qualitatively different cycle types. Our results show that during conception cycles male mating behaviour was concentrated around the fertile phase implying that males inferred information from more than swelling size alone. Male mating frequency increased in line with female socio-sexual behaviour, namely female presenting and the frequency of copulations with copulation calls. Most strikingly our results show that males invested equally in mating during fertile and non-fertile, i.e. post-conception, maximum swelling phases. Whether post-conception swellings were merely a result of changes in hormone concentrations during pregnancy or part of a female reproductive strategy remains elusive. In sum, this study adds to the body of research on the evolution of female sexual signals and how males may infer information from these cues.

Male and female reproductive strategies and multiple paternity in the polygynandrous Alpine Accentor Prunella collaris

Five breeding groups of the Alpine Accentor were studied in a Swiss alpine region. The studied groups showed a polygynandrous mating system and each group was formed of 1–4 females and 3–5 males. The females had exclusive territories, while the males cooperated in defending their group territory. Among the males of one group, a linear dominance relationship was usually well established among the alpha, beta and subordinate male S 1. Both frequent copulation and mate guarding strategies were applied. Females advertised their fertility, solicited most of the copulations and mated multiple times with several males. With approximately 350 matings during the short fertile period of 10 days, the Alpine Accentor is one of the bird species with the highest copulation frequency. Intensity of mate guarding and copulation frequency were highest starting 1 day before egg-laying and throughout the egg-laying period. The alpha male guarded a fertile female closely during the ovulation period, while the beta and other subordinate males (S 1, S 2 and S 3) were restricted in their access to fertile females by the alpha male’s mate guarding ability. In most cases, they did not guard mates and solely performed the frequent copulation strategy. Accordingly, higher ranking males got more solicitations from females, maintained a higher copulation frequency, but also refused a greater portion of all mating offers. Sperm competition was intense with 81.8 % of the broods having multiple paternity. The share of matings during the ovulation period best reflected the achieved share of paternity. Alpha, beta and S 1 sired most of the young, while S 2, S 3 and extra-group males were seldom fathers of offspring. At one nest, up to 4 males helped to feed the young, however, usually at a low rate and the overall male help (28 %) was smaller than the female contribution (72 %). In this polygynandrous mating system, females of the studied population lacked full male help but might have benefited from the greater genetic variation of their young, while males have a large individual variance in their lifetime reproductive success with higher ranking males raising their fitness to above average.

Chronic pre-exposure to methamphetamine following 31 days of withdrawal impairs sexual performance but not sexual conditioning in male Japanese quail

In the current study, male quail were administered methamphetamine (3.0 or 5.6 mg/kg IP) or saline once daily for 10 days and locomotor activity was assessed. Following a 31-day withdrawal period, sexual conditioning trials were conducted such that a conditioned stimulus (CS) was presented prior to a copulatory opportunity with a female quail. Male quail treated with methamphetamine (5.6 mg/kg) showed a decrease in locomotor activity from Trial 1 to Trial 10 suggesting a potential tolerance effect. Following the 31-day withdrawal period, all male quail that received the CS paired with a copulatory opportunity showed enhanced approach to the CS, regardless of treatment history. Thus, chronic pre-exposure to methamphetamine did not alter sexual conditioning. In contrast, chronic pre-exposure to methamphetamine (3.0 mg/kg) decreased the frequency of successful copulations suggesting that it impaired sexual performance. The findings suggest that methamphetamine may differentially affect the neural circuitry involved in motivational systems compared with those involved in consummatory aspects of sexual behavior. These effects may last long after drug cessation.

Mating Behavior and Performance in the Two Cosmopolitan Mealybug Species Planococcus citri and Pseudococcus calceolariae (Hemiptera: Pseudococcidae)

Mating strategies of mealybugs were investigated using two heterogeneric cosmopolitan species as case study: Planococcus citri (Risso) and Pseudococcus calceolariae (Maskell). Male mating behavior of the studied species differed in respect to mate selection, and frequency and duration of copulation. Females played an active role in mate selection, by either facilitating or resisting copulation. This is a first evidence of female sexual active behavior in scale insects. In both species, male predisposition to mate was affected by previous exposition to light. The frequency of courtship and copulation decreased with the age of females for Pl. citri but not for Ps. calceolariae. Mating frequency increased with female colony density in both species.

Seasonality of reproduction of wild black-and-white snub-nosed monkeys (Rhinopithecus bieti) at Mt. Lasha, Yunnan, China

Black-and-white snub-nosed monkeys (Rhinopithecus bieti) inhabit one of the harshest habitats by any nonhuman primate. Reliable predictive cues to initiate reproduction may be particularly critical for R. bieti because they inhabit such seasonally energetically challenging environments. To better understand the seasonal distribution of and predictive cues to reproduction, we collected breeding and birth data in a population of R. bieti at Mt. Lasha in Yunling Nature Reserve, Yunnan, China, from January 2008 to May 2010, using a combination of 10-min instantaneous scans and ad libitum observations. We examined variations in temperature, rainfall, and food availability, as well as photoperiod differences between Mt. Lasha and the more northerly Xiaochangdu to identify environmental influences on the timing of reproductive events. Our data show the area exhibited distinct seasonal fluctuations in rainfall, temperature, and food availability. Mating occurred year-round, but peaked in August, coinciding with the end of the period of highest temperatures and food availability, and during the peak rainfall. Copulation frequency peaked 1 month after corresponding peaks in staple foods, rainfall, and minimum temperatures, and 3-4 months after peaks in high-quality foods. Births were significantly seasonal, with a birth peak from mid-February to early April, and a mean birth date of 14 March. Eleven births occurred in 41 days in 2009, and 16 births occurred in 52 days in 2010. Births occurred during periods of increasing temperatures and food availability. Our findings are suggestive of at least one environmental control of conception timing, and support the notion that food availability during key reproductive stages is an ultimate factor for birth seasonality, but provide no supporting evidence for photoperiod during the conception season as a proximate cue to reproduction in R. bieti.

Predation risk suppresses mating success and offspring production in the coastal marine copepod, Eurytemora herdmani

We investigated the effects of a common mysid predator, Neomysis americana on the mating success of an estuarine copepod, Eurytemora herdmani. The presence of a mysid predator, or only a predator cue, reduced copulation frequency and spermatophore transfer success of E. herdmani. and led to a substantial decrease in E. herdmani nauplius production. Thus, mysid predators can influence copepod population growth through nonconsumptive processes by reducing the frequency and success of mating events. This highlights the need to look beyond population‐level demographic factors (i.e., sex ratio and population density) and consider community‐level ecological factors (such as predation risk) when modeling population growth rates of prey species critical to marine food webs.

Why fight? Selective forces favoring between-group aggression in a variably pair-living primate, the white-faced saki (Pithecia pithecia)

Between-group aggression is a common feature of many group-living animals. Yet aggressive behaviors are often costly, involving risk of injury, increased energy expenditure and the potential to reduce feeding time. For aggression to be evolutionarily advantageous these costs must be outweighed by the benefits gained from exclusive access to resources and/or mates, or through committing infanticide. However, the dynamics favoring aggression in species living in small groups may differ from those in larger groups since mating exclusivity is higher and the potential to numerically dominate opponents is lower. We examined the selective factors influencing between-group aggression in a primate that lives in both pairs and small groups, the white-faced saki monkey (Pithecia pithecia). Data were collected on three free-ranging groups at Brownsberg Naturepark (Suriname) over 17 months. Intergroup encounter frequency and intensity of aggression during encounters were compared to temporal changes in diet, variation in ovarian hormones, frequency of copulations and the presence of dependent infants. Participation in between-group aggression was heavily male-biased and the presence of cycling females was a significant predictor of aggression frequency. Percentage of mesocarp in the diet also had a significant effect on the frequency and the intensity of aggression, with high mesocarp consumption corresponding to increased aggression. Presence of dependent infants did not affect between-group aggression. Our results support both the male mate defense and male resource defense hypotheses, suggesting that male reproductive interests are the principle selective pressures acting on between-group aggression in white-faced sakis. White-faced sakis’ rigid conformity to traditional expectations of male intrasexual intolerance appears to be unique among primates living in small groups with variable mating systems.

Reproductive Biology, Mating Behavior, and Vibratory Communication of the Brown-Winged Stink Bug,Edessa meditabunda(Fabr.) (Heteroptera: Pentatomidae)

We describe different aspects of the reproductive biology, mating behavior, and vibratory communication of the pentatomidEdessa meditabunda(Fabr.). This species shows lower copulation frequency and reproductive potential with longer sexual maturation period compared to other species of pentatomids. Females with multiple mating show increased fecundity when compared with single-mated females and both increased fecundity and reduced longevity when compared with virgin females. Courtship and mating behavior and vibratory signals are typical and similar to what was observed in other species of pentatomids, except that males started the courtship. These results constitute the first paper on biology, behavior, and vibratory communication among species of the subfamily Edessinae.

The Evolution of Large Testes: Sperm Competition or Male Mating Rate?

AbstractA positive relationship across species between the extent to which females mate with more than one male and relative testes mass has been demonstrated in a wide range of vertebrate taxa and certain insects. At least two hypotheses, which are not necessarily mutually exclusive, could account for this pattern: (1) the numerical sperm competition hypothesis, which assumes that larger testes enable the male to transfer more sperm to each female, giving the male an advantage in sperm competition and (2) the male mating rate hypothesis, which proposes that larger testes allow the male to produce a greater number of (potentially smaller) ejaculates to engage in frequent copulations with different females. Of these hypotheses, the former has won broad acceptance, while the latter has tended to be dismissed. Here, we argue that the lines of evidence commonly used to support the numerical sperm competition hypothesis in favour of the male mating rate hypothesis are not as clear cut or generally applicable as they are purported to be and that, consequently, the male mating rate hypothesis cannot be excluded with confidence on the basis of the current evidence. Furthermore, some evidence, such as the finding that ejaculate mass and/or sperm number is negatively correlated with testes mass across species in some insects and that larger testes in Drosophila can evolve in response to an increase in the number of females available for mating in the laboratory, provides support for the male mating rate hypothesis. Further work is needed to disentangle the relative effects of these selective pressures on the evolution of testes size.

Laying-order effects on sperm numbers and on paternity: comparing three passerine birds with different life histories

In birds, the number of sperm trapped between the perivitelline membranes around the ovum is an estimate of sperm numbers present at the time and place of fertilisation in the female reproductive tract. Sperm numbers may vary among species and between eggs in a clutch and can provide information about sperm utilisation and mechanisms of sperm competition. Here, we describe patterns of variation in sperm numbers through the egg-laying sequence in three passerines in which extra-pair paternity is common, but copulation behaviour differs. Sperm numbers showed no systematic change across the laying sequence in blue tits (Cyanistes caeruleus), but decreased significantly with laying order in bluethroat (Luscinia svecica) and tree swallow (Tachycineta bicolor) clutches. This is consistent with observations that blue tits regularly copulate throughout the laying sequence, while bluethroats stop mate guarding and tree swallows reduce their copulation frequency once the first egg is laid. Nevertheless, cases of a sudden increase in sperm numbers in clutches of bluethroats and tree swallows suggest that successful inseminations also occurred after laying started. In blue tits and bluethroats, sperm numbers were not higher on extra-pair sired eggs than on eggs sired by the social male, suggesting that extra-pair copulations are not timed to the period of peak fertility for each egg. More extra-pair offspring originated from eggs laid early in the sequence in blue tits, while there was no systematic bias in bluethroats. Our results suggest that copulations during the laying sequence are predominantly performed by within-pair males in our study species.

Breeding ecology of the Twite Carduelis flavirostris in northern Tibet

The breeding ecology of the Twite was studied during 2004-2007 in a meadow environment at 4,300 m elevation, in northern Tibet. Twite laid eggs between late May and mid-August in response to ripeness of seed food. Nests were located in firewood stacks, trees and marshes, with average inter-nest distances less than 15 m. Pairs formed monogamously and males used both proximity and frequent copulations to guard their paternity. Clutch size averaged 4.2 (± 0.7 SD; 3-7), seasonally increasing or remaining unchanged according to year. Incubation by the female only lasted 12.2 days (± 1.2 SD; 10-15) and provisioning of chicks in the nest was continued by both parents for 14.7 days (±1.1 SD; 7 13-17). Males performed courtship feeding when their mates were engaged in egg-laying, incubating and brooding. Breeding success, measured as the percentage of nesting attempts from which at least one nestling fledged, was 64%. Compared to their lowland counterparts, Tibetan Twite produced smaller clutches and larger eggs, suggesting a life history strategy to cope with the harsh high-elevation environment.

Copulatory pattern and behavior in a semi-captive population of Eld’s deer

Abstract Male copulatory patterns, female multiple copulation and male post-copulatory guarding were studied in Eld’s deer Cervus eldi in Datian National Nature Reserve, China. Mating behavior in 18 females and 11 males from a group of 61 semi-captive Eld’s deer were observed. The majority (55.8%) of copulations occurred between 15:00–19:00 h. The ejaculatory mount was preceded by an average of 5.1 prior mounts. Successful copulation consisted of a single thrust with ejaculation during one intromission, with no lock. This copulatory pattern is classified as pattern No. 15 (no lock, no intravaginal thrusting, single intromission, and multiple ejaculation) and No. 16 (no lock, no intravaginal thrusting, single intromission, and single ejaculation) under Dewsbury’s scheme (1972) and as No. 16 (no lock, no thrusting, single and brief intromission) under Dixson’s classification (1998). Copulation frequency was 1.5 ± 0.9 times for males/ females with the same female/male per day. The duration of the final mount, which included ejaculation, was brief (3.4 ± 1.3 s), and ejaculation usually terminated copulation. Eleven females copulated more than once in this study: three of them copulated with several males (multi-male copulations) and the remainder copulated with a single male (repeated copulations). Our results indicate that some female Eld’s deer may seek multiple copulations to be a strategy to improve the genetic quality of their offspring or to avoid harassment. Post-copulatory guarding of females by males followed all copulations, with dominant males guarding for significantly longer than subordinate males. Dominant males appear to be more effective at post-copulatory guarding than subordinate males. Subordinate males engaged in a quicker pre-copulatory phase to improve their chances of finishing copulation before being forced to accede to dominant males.

Mate choice opportunity leads to shorter offspring development time in a desert insect

We describe indirect genetic benefits of mate choice in two allopatric populations of cactophilic Drosophila mojavensis. By manipulating mate choice opportunity, we show that greater mate choice among sexually mature adults leads to shorter offspring egg-to-adult development times; the extent of this reduction was influenced by population origin and by host plant environment. We performed multiple-choice mating trials with individually marked flies to investigate whether differential male mating success was a consequence of female choice, male interaction, or both. We demonstrate that male copulation frequency was not random and instead, was determined by female choice. Virgin females in these trials were no less discriminating than females that had been previously exposed to males. These results suggest that there are indirect benefits of female mate choice that are population and environment specific, consistent with the hypothesis of ecologically influenced 'good genes' sexual selection.

Leaf substrates determine oviposition and in turn frequency of copulation in the whitefly Bemisia tabaci

Leaf substrates determine oviposition and in turn frequency of copulation in the whitefly Bemisia tabaci

Persistent Copulation in Asexual Female Potamopyrgus antipodarum: Evidence for Male Control with Size-Based Preferences

Transitions from sexual to asexual reproduction provide a useful context for investigating the evolutionary loss of nonfunctional traits. It is often assumed that useless behaviors or structures will degrade, but this process is poorly understood. Potamopyrgus antipodarum is an ancestrally sexual New Zealand freshwater snail characterized by numerous independent transitions to asexual all-female lineages. The availability of multiple independently-derived asexual lineages of various time since derivation from sexual ancestors means that the P. antipodarum system is well-suited for the study of trait loss related to mating behavior and copulation. Here, we asked whether mating behavior in asexual female P. antipodarum degrades with increasing asexual lineage age. While copulation frequency did not differ in females from old versus young asexual lineages, post hoc analyses indicated that it was instead positively associated with mean lineage female size. We observed that female P. antipodarum take a passive physical role in copulatory interactions, indicating that female behavior may not be a useful variable for detection of sex-related vestigialization in this system. Instead, males seem to be in proximate control of copulation frequencies, meaning that male mating behavior may be a primary determinant of the expression of mating behavior in asexual female P. antipodarum.

Fruitless RNAi knockdown in males interferes with copulation success in Schistocerca gregaria

In Drosophila melanogaster, the male-specific splice isoform of the fruitless gene ( Fru M ) codes for a set of transcription factors that are involved in the regulation of male courtship and copulation. Fru M is expressed in an interconnected neuronal circuit containing central and sensory neurons as well as motor neurons. A partial sequence from the Schistocerca gregaria fru-gene from an EST database allowed quantitative real time analysis of fru-expression in adult locusts, and revealed the highest expression in the testes, accessory glands as well as the brain (and optic lobes). Starting fru specific RNAi knockdown in the third and fourth nymphal stage resulted in a significantly lower cumulative copulation frequency of the RNAi-treated animals compared to controls after 3 h of observation. In addition, the testes of RNAi-treated males weigh less. Analysis of the egg pods resulting from a successful copulation event revealed that egg pods from females that mated with an RNAi-treated male were smaller and contained less fertilized eggs compared to egg pods from females who mated with control males. Starting injections in the fifth nymphal stage showed the complete opposite for the cumulative copulation frequency and testes weight. We conclude that already in the early nymphal phases of male desert locusts, fruitless starts to play an important role in the regulation of successful copulation in the adult. The RNAi treatment in the male has also its effects on fertility and fecundity. It remains unknown whether this effect is coming from aberrant courtship behaviour or from an altered composition of the sperm or seminal fluids.

Paternity analysis in an egg-carrying aquatic insect Appasus major (Hemiptera: Belostomatidae) using microsatellite DNA markers

The giant water bug Appasus major exhibits a peculiar reproductive behavior where females lay eggs on the backs of males. A male and female pair performs frequent repeat copulations during the oviposition behavior, and the male carries the deposited eggs until hatching. Such characteristic behaviors predict that the eggs are fertilized by the brooding males. If males carry eggs of other unrelated males, the egg carrying will drastically decrease the fitness of the carriers. In this study, we examined genetic relationships between the 489 eggs and nine males carrying them collected from the field, using microsatellite DNA markers. We revealed that in total, 28.4% of the eggs were of other male origin. This is the first report of frequent brood parasitism in an aquatic egg-carrying hemipteran insect. The brood parasitism is adaptive for the females probably because it enables them to increase the chance of oviposition, or it can equalize motility risk of the eggs of each mate.

Effects of egg testosterone on female mate choice and male sexual behavior in the pheasant

Evidence is accumulating that sex steroids in the eggs, besides affecting progeny phenotype and behavior in the short term, also have enduring effects until adulthood, when they may translate into differences in reproductive strategies and success. Maternal steroids transfer may therefore affect both agonistic behavior and mate choice decisions, either through the promotion of body size and condition or through a priming effect on the neuroendocrine system. However, owing to the prevalence of a short-term perspective, relevance of maternal transfer of sex steroids to sexual selection processes has been seldom studied. Here we investigate the effects of an experimental increase in egg testosterone on male dominance and copulation success in the ring-necked pheasant, Phasianus colchicus, a polygynous galliform with multiple male ornamental traits, in captivity. We found that females from testosterone (T) injected eggs copulated less than control females. Males from T-injected eggs obtained more copulations than control males, specifically with control females. The effect of male ‘ordinary’ and secondary sexual traits on either dominance or copulation frequency did not depend on early exposure to T, nor did T treatment affect male dominance. Present results demonstrate that variation in the early hormonal environment set up by mothers affects sexual behavior of the offspring, which might translate into fitness differences.

Estrous asynchrony causes low birth rates in wild female chimpanzees

Estrous cycle asynchrony likely functions to elevate individual females' sexual attractiveness during female mate choice. Female chimpanzees show physiological estrus as anogenital swelling. Copulations are concentrated during the period of maximal tumescence, which is called the estrous period. A group of female chimpanzees in Mahale Mountains National Park, Tanzania, was shown to display asynchrony in both maximal tumescence and periovulatory periods. We tested the hypothesis that females establish asynchronous maximal tumescence or periovulatory periods with respect to other females to increase copulation frequency and birth opportunities (Hypothesis 1). We analyzed differences in birth rates between four asynchronous years and five nonasynchronous years. Counter to Hypothesis 1, females in periovulatory periods during asynchronous years showed significantly lower birth rates than those in nonasynchronous years. In addition, periovulatory females copulated more frequently on days on which no other female in a periovulatory period was present. These results suggest that birth rates tend to decrease when females experience nonoverlapping ovulation cycles, although copulation frequency is high. Such a decrease in the birth rate may have resulted from the cost associated with multiple copulations. We tested two other hypotheses: paternity confusion (Hypothesis 2) and sperm competition (Hypothesis 3). Both of these hypotheses were partially supported. The highest-ranking male most effectively monopolized access to receptive females when relatively few other males and receptive females from the party (or subgroup) were present. The viability of Hypotheses 2 and 3 requires that dominant males are able to hinder a female from mating with other males. Given that the male-biased operational sex ratio created by female asynchrony is likely to reduce the efficiency of mate guarding by dominant males, an asynchronous female may gain a fitness benefit by increasing the probability of mating with at least one male who produces superior sperm.