Copulation duration, insemination efficiency and male attractiveness in guppies

doi:10.1016/j.anbehav.2006.09.016

Animal Behaviour

Volume 74, Issue 2, August 2007, Pages 321-328

https://doi.org/10.1016/j.anbehav.2006.09.016 Get rights and content

In polyandrous species, females may influence paternity by biasing sperm usage in favour of particular males. In the guppy, Poecilia reticulata, the number of sperm inseminated in a copulation depends on the female's perception of male attractiveness. We videorecorded copulations in the laboratory to test the hypothesis that there is a positive correlation between the number of sperm inseminated and the duration of the copulation. Duration was positively correlated with the number of sperm retrieved from the female's gonoduct. Once copulation duration was statistically controlled for, more sperm were retrieved from the gonoduct in courtship copulations than in coercive copulations, and in postpartum females than in virgin females. Copulation duration was positively correlated with the degree of carotenoid coloration of the male, suggesting that copulation duration might be the proximate mechanism of cryptic female choice in this species. The intensity of ‘jerking’, a postcopulatory behaviour of male guppies, was positively correlated with the number of sperm inseminated, suggesting a possible signalling function of this display.

Section snippets

Experimental Fish

The guppies used in this experiment were descendents of fish caught in the Tacarigua river, Trinidad (10°40.736′N, 061°19.168′W) in 2002. The males were reared in several mixed-sex 150-litre aquaria (ca. 1:1 sex ratio) until required. Water temperature was maintained between 25 and 27°C and illumination was set on a 12:12 h light:dark cycle (Philips TLD 36 W fluorescent lamps). All fish were fed a mixed diet of brine shrimp nauplii and commercially prepared flake food. Before mating, males were

Results

We obtained 31 matings, 21 with virgin females and 10 with postpartum females. Table 1 gives the descriptive statistics of the matings. Twenty-six of the matings were courtship copulations and five were sneaky copulations (i.e. the male approached the unaware female from behind and thrust his gonopodium towards her genital pore). Sneaky copulations were significantly shorter $(\bar{X} \pm SD = 0.01 \pm 0.03 s)$ than courtship copulations (0.72 ± 0.41 s; Student's t test: t₂₉ = 5.72, P < 0.0001). The duration of the

Discussion

Pilastro et al. (2004) showed that the number of sperm transferred during copulation in guppies depends on the female's perception of mate attractiveness, suggesting that sperm transfer is partially under female control. The results of the present study show that the number of sperm found in the female's gonoduct after copulation depends on copulation duration, suggesting that copula interruption may be the mechanism used by female guppies to control the number of sperm inseminated. This

Acknowledgments

We thank David Cirelli for his help with mating trials and Giorgio Bertorelle for useful discussion on jerking as an honest signal. Jon Evans and two anonymous referees provided useful comments on the manuscript. This study was funded by grants from the University of Padova (Progetto di Ateneo CPDA031972 to A.P.; Ricerca Scientifica Ex-60% 2003–5 to A.B. and A.P.).

References (61)

J.A. Andres et al.
Copulation duration and fertilization success in a damselfly: an example of cryptic female choice?
Animal Behaviour
(2000)
C.C. Bozynski et al.
The effect of female presence on spermiation, and of male sexual activity on ‘ready’ sperm in the male guppy
Animal Behaviour
(2003)
G.D. Constantz
Sperm competition in Poeciliid fishes
J.P. Evans et al.
Male mating behaviour and sperm production characteristics under varying sperm competition risk in guppies
Animal Behaviour
(1999)
T.L. Karr et al.
Sperm competition: defining the rules of engagement
Current Biology
(1999)
M. Olsson et al.
Sexual selection and sperm competition in reptiles
R. Pocklington et al.
Predation on females or males: who pays for bright male traits?
Animal Behaviour
(1995)
L.W. Simmons et al.
Sperm competition in insects: mechanisms and the potential for selection
R.R. Snook
Sperm in competition: not playing by the numbers
Trends in Ecology and Evolution
(2005)
S.R. Telford et al.
Establishing cryptic female choice in animals
Trends in Ecology and Evolution
(1998)

N. Wedell et al.

Sperm competition, male prudence and sperm-limited females

Trends in Ecology and Evolution

(2002)

J.A. Alipaz et al.

Gametic incompatibilities between races of Drosophila melanogaster

Proceedings of the Royal Society of London, Series B

(2001)

S.A. Becher et al.

Multiple mating and reproductive skew in Trinidadian guppies

Proceedings of the Royal Society of London, Series B

(2004)

T.R. Birkhead et al.

Sperm Competition and Sexual Selection

(1998)

T.R. Birkhead et al.

Postcopulatory sexual selection

Nature Reviews Genetics

(2002)

R. Brooks

Melanin as a visual signal amplifier in male guppies

Naturwissenschaften

(1996)

R. Calsbeek et al.

Within-clutch variation in offspring sex determined by differences in sire body size: cryptic mate choice in the wild

Journal of Evolutionary Biology

(2004)

E. Clark et al.

Sexual behavior in the guppy, Lebistes reticulatus (Peters)

Zoologica

(1951)

G.D. Constantz

Reproductive biology of Poeciliid fishes

D.A. Dewsbury

Ejaculate cost and male choice

American Naturalist

(1982)

W.G. Eberhard

Female Control: Sexual Selection by Cryptic Female Choice

(1996)

M. Edvardsson et al.

Copulatory courtship and cryptic female choice in red flour beetles Tribolium castaneum

Proceedings of the Royal Society of London, Series B

(2000)

M.A. Elgar et al.

Female control of paternity in the sexually cannibalistic spider Argiope keyserlingi

Proceedings of the Royal Society of London, Series B

(2000)

J.A. Endler et al.

Geographic variation in female preferences for male traits in Poecilia reticulata

Evolution

(1995)

J.P. Evans et al.

Patterns of sperm precedence and predictors of paternity in the Trinidadian guppy

Proceedings of the Royal Society of London, Series B

(2001)

J.P. Evans et al.

Sperm transfer through forced matings and its evolutionary implications in natural guppy (Poecilia reticulata) populations

Biological Journal of the Linnean Society

(2003)

J.P. Evans et al.

Directional postcopulatory sexual selection revealed by artificial insemination

Nature

(2003)

J.P. Evans et al.

Female mating preferences for colourful males in a population of guppies subject to high predation

Journal of Fish Biology

(2004)

M. Gomendio et al.

Sperm competition in mammals

A.E. Houde

Sex, Color, and Mate Choice in Guppies

(1997)

Cited by (74)

Trade-offs of strategic sperm adjustments and their consequences under phenotype–environment mismatches in guppies
2020, Animal Behaviour
Citation Excerpt :
With a Gilson pipette, we measured the volume of the solution drained from the female and we diluted it 1:5 in saline solution. We counted the sperm contained in the solution using an ‘improved Neubauer chamber’ haematocytometer under an optical microscope (at magnification ×400; Pilastro, Evans, Sartorelli, & Bisazza, 2002; Pilastro et al., 2007). The reliability of this technique was proved in previous studies (Pilastro et al., 2007), which demonstrated that the number of sperm retrieved from the female is significantly correlated with the number of sperm inseminated.
In polyandrous species males invest significant resources in producing large and high-quality ejaculates. As ejaculates are costly, males are expected to modulate their investment in response to social cues associated with the expected level of sperm competition or mating opportunity, to anticipate future mating conditions. Another consequence of ejaculate costs is that the increase in ejaculate production may be traded against traits linked to mate acquisition. In such cases, the effect of this anticipatory plasticity in ejaculate investment on a male's reproductive success will depend on the balance between postcopulatory benefits and precopulatory costs in the sociosexual context subsequently encountered. Here, we used the guppy, Poecilia reticulata, a live-bearing fish characterized by intense sperm competition, to investigate how mismatches between anticipatory phenotypes and the social conditions subsequently experienced affect male reproductive success. Male guppies kept in visual contact with females, a social stimulus predicting high mating opportunities, increase their sperm production compared to female-deprived males which foresee fewer opportunities to mate, but simultaneously reduce their courtship rate. Using a paired experimental design, we manipulated the male's perceived mating opportunities by housing them in the presence (FP) or in the absence (FA) of females. We then measured male mating and insemination success under two conditions: (1) a female-biased sex ratio, matching expected FP cues; and (2) a male-biased sex ratio, matching expected FA cues. Under a female-biased sex ratio, mating and insemination success were not affected by previous exposure to females, although FP males experienced a lower risk of sperm depletion after several copulations. However, FP males showed a small, but significant, reduction in their mating success under a male-biased sex ratio, when directly competing with an FA male. Males showed significant repeatability in mating and insemination success within a sex ratio context, suggesting that the costs of mismatching anticipatory ejaculate responses are probably low in this species.
Relative sexual attractiveness does not influence mate-choice copying in male Trinidadian guppies, Poecilia reticulata
2020, Animal Behaviour
Citation Excerpt :
Although there is some evidence for last-male sperm precedence in the Trinidadian guppy (Evans & Magurran, 2001; Gasparini & Evans, 2018; Neff & Wahl, 2004; Pilastro, Mandelli, Gasparini, Dadda, & Bisazza, 2007; Pilastro et al., 2004) when females mate naturally and sequentially with different males, such apparent last-male sperm precedence may alternatively be explained by female control over sperm transfer and use in egg fertilization, biased towards the perceived sexually more attractive male (Evans, Zane, Francescato, & Pilastro, 2003; Gasparini & Evans, 2018; Pilastro, Simonato, Bisazza, & Evans, 2004), rather than male insemination order per se. Studies using artificial insemination in the guppy (Evans et al., 2003; Magris, Cardozo, Santi, Devigili, & Pilastro, 2017), which disentangle the effect of female control over copulation duration, sperm transfer and fertilization (Boschetto, Gasparini, & Pilastro, 2011; Pilastro et al., 2004, 2007) from the effect of male insemination order, have shown either no order effect or first male precedence when artificial inseminations of sperm from two males occur within 24 h (which is the time frame relevant to the mate-choice copying context). In the guppy, females have considerable control over the number of sperm transferred during cooperative copulations (Pilastro et al., 2004, 2007), and the number of sperm transferred strongly predicts a male's sperm competition success (Boschetto et al., 2011).
Copying the mate choice of another conspecific by a bystanding observer is a socially mediated alternative mating strategy to independent mate choice. Because increased sperm competition is a potential cost of mate-choice copying, males should be prudent and less likely to copy the observed mate choice of other males when the latter are more sexually attractive than themselves. We tested this hypothesis using the Trinidadian guppy, Poecilia reticulata. Focal observer males were simultaneously presented with a large and a small female as potential mates, either in the presence or absence of a nearby model male. We varied the relative differences in the body length and colour ornamentation, traits that predict male sexual attractiveness and competitiveness in the guppy, of observer and model males in each of three experimental treatments: (1) observer and model males were matched for body length and colour ornamentation; (2) the model male was larger and more colourful than the observer male; (3) the model male was smaller and less colourful than the observer male. We compared the mating preferences of focal observer males in each of the latter treatments with that of focal males in a control treatment, wherein no model male (and thus no copying opportunity) was present. As predicted, focal males copied the staged apparent mate choice of a model male in all three experimental treatments, but not in the control treatment. However, contrary to our a priori hypothesis, there were no significant differences in the likelihood or strength of the copying response in observer males among the experimental treatments. Although male guppies are known to modify their mating tactics in the presence of sexual competitors, we found no evidence for an influence of the relative phenotypes of observer and model males on mate-choice copying behaviour in focal observer males.
Female guppies increase their propensity for polyandry as an inbreeding avoidance strategy
2019, Animal Behaviour
Citation Excerpt :
In addition to recording the number of courtship displays, we also recorded the number of ‘postcopulatory jerks’ performed by each male after a mating. In addition to signalling successful sperm transfer (Houde, 1997), the frequency of postcopulatory jerks is also useful as a proxy for the number of sperm transferred during the mating, as the number of jerks is positively correlated with the amount of sperm transferred (Pilastro, Mandelli, Gasparini, Dadda, & Bisazza, 2007). After the copulation, the focal male was removed, and the female was given 1 h to recover.
Mating with close relatives often causes a decline in offspring fitness, termed inbreeding depression. Consequently, pre- and postcopulatory inbreeding avoidance mechanisms are likely to evolve, especially in females due to their relatively high levels of reproductive investment. If precopulatory inbreeding avoidance mechanisms are absent or unreliable, females may exploit postcopulatory sexually selected inbreeding avoidance mechanisms by mating with multiple males (polyandry). Despite this expectation, few studies have tested whether females alter their propensity to mate multiply in an inbreeding avoidance context. Here, we tested whether the perceived risk of inbreeding promotes polyandrous behaviour in guppies, Poecilia reticulata, a species susceptible to inbreeding depression. Virgin females were assigned to either a sibling or nonsibling mating and subsequently presented with three unrelated males simultaneously. Consistent with previous studies, we found that females did not discriminate between initially encountered males based on relatedness. However, females increased their propensity to mate multiply after mating with a brother. Subsequent paternity tests were performed to determine whether polyandry minimizes inbreeding through a dilution effect (i.e. greater number of sires in the related treatment) or through postcopulatory biasing mechanisms (i.e. greater paternity skew towards unrelated males). Surprisingly, our results supported neither scenario; we detected no significant difference in paternity skew or the number of sires between treatments. Overall, our study provides a rare example of females responding to an increased risk of inbreeding by increasing their propensity to remate, but the postcopulatory processes arising from this behaviour, along with the mechanisms underlying kin recognition, await further investigation.
2,2′-Dithiobis-pyridine induced reproductive toxicity in male guppy (Poecilia reticulata)
2019, Ecotoxicology and Environmental Safety
Metal pyrithiones (MePTs) are frequently used antifouling biocides in marine coatings. Their main degradation product, 2,2′-dithiobis-pyridine ((PS)₂), has been widely detected in seawater and may pose potential ecological risks. In the present study, sexually mature guppies (Poecilia reticulata) were exposed to (PS)₂ at concentrations of 0, 20, 200, and 2000 ng/L for 28 days to investigate its reproductive toxicity. The results showed that (PS)₂ significantly reduced testosterone (T) levels, spermatogenic cyst number and sperm motility, impeded spermatogenic cell differentiation in male guppies and delayed embryo development in females. These results indicated that (PS)₂ could cause reproductive toxicity in guppies. We also examined mRNA expression of indices involved in the hypothalamic–pituitary–gonadal axis and reproductive behaviors. We found that 200 and 2000 ng/L (PS)₂ decreased T synthesis by downregulating 17βHSD and CYP17 mRNA levels, and upregulating the mRNA level of CYP19a1a, which converted T to 17β-estradiol. (PS)₂ also upregulated GnRH1, FSHβ, LHβ, and LHR mRNA levels, a positive feedback regulation due to the decrease of T levels in male guppies. Furthermore, (PS)₂ significantly decreased CYP19a1b mRNA levels in all three exposure groups and thus reduced the display frequency of male guppies. This study was the first to report that (PS)₂ could induce reproductive toxicity, which would provide a basis for future assessment of its ecological risk.
The pharmaceutical pollutant fluoxetine alters reproductive behaviour in a fish independent of predation risk
2019, Science of the Total Environment
Pharmaceutical pollutants constitute a major threat to wildlife because of their capacity to induce biological effects at low doses. One such pollutant is the antidepressant fluoxetine, which has been detected in surface waters globally at levels that recent studies suggest can alter physiology and behaviour in aquatic organisms. However, wildlife exposed to pharmaceutical contaminants are typically confronted with multiple stressors simultaneously, including predation risk, which is a particularly important natural stressor that can have direct (e.g. mortality) and indirect (e.g. changed prey behaviour) fitness effects. Accordingly, we investigated potential impacts of environmentally realistic fluoxetine exposure on reproductive behaviour in the guppy (Poecilia reticulata) under predation risk. Specifically, we tested whether fluoxetine exposure altered mating behaviour in male and female guppies in the presence of either a predatory spangled perch (Leiopotherapon unicolor) or a non-predatory rainbowfish (Melanotaenia splendida) control. We found that fluoxetine and the presence of a predatory spangled perch did not interact to affect reproductive behaviour. We also found that, independent of a predatory threat, fluoxetine exposure altered male mating strategy, with males in the high treatment conducting significantly more coercive ‘sneak’ copulations, whereas the number of courtship displays performed was not significantly affected. Moreover, while fluoxetine exposure did not significantly affect the amount of time that males and females spent following one another, we found that females, but not males, followed a potential partner less when in the presence of the predatory fish. Finally, both sexes reacted to the risk of predation by spending less time in close proximity to a predator than a non-predator. In combination, our findings highlight the capacity of fluoxetine to influence processes of sexual selection at field-realistic concentrations and emphasise the importance of considering multiple stressors when assessing impacts of pharmaceutical pollutants on the behaviour of wildlife.
Sexual selection on the multicomponent display of black morph male Girardinus metallicus (Pisces: Poeciliidae)
2018, Behavioural Processes
Sexually selected displays often include suites of integrated traits. Black morph males of the poeciliid fish Girardinus metallicus perform courtship and aggressive displays that exhibit their conspicuous yellow and black coloration. Body size, gonopodium size and ventral black area are correlated with intermale aggression, which is key for access to mates. A previous study showed that females may prefer dominant males prior to watching them fight; however, that result was obtained in trials that allowed for male-male interactions across partitions, and to date no study has uncovered the traits important in female choice. We performed a more comprehensive investigation of the multicomponent sexual display including measures of male yellow hue, saturation and brightness. We examined the behavior of size-matched males paired to maximize the difference in yellow saturation, and measured female choice exclusive of male-male interactions and chemical cues. We found no female preference for any traits in the multicomponent sexual display. Males with brighter and more saturated yellow coloration were more likely to be dominant, and dominant males courted and attempted copulations more. Our results suggest that yellow coloration is sexually selected; however, the courtship display requires further investigation because we did not identify targets of female preference, and we discuss possible explanations for this finding.

View all citing articles on Scopus

View full text

Copulation duration, insemination efficiency and male attractiveness in guppies

Section snippets

Experimental Fish

Results

Discussion

Acknowledgments

Animal Behaviour

Animal Behaviour

Animal Behaviour

Current Biology

Animal Behaviour

Trends in Ecology and Evolution

Trends in Ecology and Evolution

Trends in Ecology and Evolution

Gametic incompatibilities between races of Drosophila melanogaster

Proceedings of the Royal Society of London, Series B

Multiple mating and reproductive skew in Trinidadian guppies

Proceedings of the Royal Society of London, Series B

Sperm Competition and Sexual Selection

Postcopulatory sexual selection

Nature Reviews Genetics

Melanin as a visual signal amplifier in male guppies

Naturwissenschaften

Within-clutch variation in offspring sex determined by differences in sire body size: cryptic mate choice in the wild

Journal of Evolutionary Biology

Sexual behavior in the guppy, Lebistes reticulatus (Peters)

Zoologica

Reproductive biology of Poeciliid fishes

Ejaculate cost and male choice

American Naturalist

Female Control: Sexual Selection by Cryptic Female Choice

Copulatory courtship and cryptic female choice in red flour beetles Tribolium castaneum

Proceedings of the Royal Society of London, Series B

Female control of paternity in the sexually cannibalistic spider Argiope keyserlingi

Proceedings of the Royal Society of London, Series B

Geographic variation in female preferences for male traits in Poecilia reticulata

Evolution

Patterns of sperm precedence and predictors of paternity in the Trinidadian guppy

Proceedings of the Royal Society of London, Series B

Sperm transfer through forced matings and its evolutionary implications in natural guppy (Poecilia reticulata) populations

Biological Journal of the Linnean Society

Directional postcopulatory sexual selection revealed by artificial insemination

Nature

Female mating preferences for colourful males in a population of guppies subject to high predation

Journal of Fish Biology

Sperm competition in mammals

Sex, Color, and Mate Choice in Guppies