Behavioral Ecology Advance Access originally published online on August 29, 2008
Behavioral Ecology 2008 19(6):1080-1086; doi:10.1093/beheco/arn105
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Seasonal plasticity in male mating preferences in sailfin mollies
a Section of Integrative Biology C0930, University of Texas, Austin, TX 78712, USA b Department of Biological and Environmental Sciences, PO Box 65, University of Helsinki, FIN-00014, Finland c Department of Zoology, University of Oklahoma, 730 Van Vleet Oval, Norman, OK 73019, USA
Address correspondence to K. Heubel, who is now at Laboratory of Ecological and Evolutionary Dynamics, Department of Biological and Environmental Sciences, PO Box 65, (Viikinkaari 1), University of Helsinki, FIN-00014, Finland. E-mail: katja.heubel{at}helsinki.fi.
Received 2 October 2005; revised 21 July 2008; accepted 23 July 2008.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
|---|
Although male choosiness may be influenced by predation risk, variation in mate availability, and fecundity that may vary spatially and over time, there is little evidence for variation in male mate choice preferences. In mixed populations of bisexual sailfin mollies (Poecilia latipinna) and unisexual Amazon mollies (Poecilia formosa), males encounter 2 types of potential mates: conspecific sexual sailfin and asexual Amazon mollies. The latter is gynogenetic, thus an all-female species that produces clonal offspring but requires sperm from sexual host males to trigger embryogenesis. Sailfin males do not benefit directly from mating with Amazon mollies, which raises the question why males mate with Amazons at all. Mate choice might be crucial in this context. So far, the possibility that male choice might vary during the mating season remained unexplored. We tested for frequency-dependent or seasonally influenced behavioral plasticity in mating preferences of males originating from natural mixed populations that may contribute to the maintenance of coexistence in this asexual–sexual mating complex. In simultaneous choice tests, we studied male association preferences in P. latipinna originating from populations in South and Central Texas, USA. There was high seasonal variation in male association patterns: males spent less time with asexual females at times that may potentially coincide with reproductive peaks in this species complex, for example, during spring. Male body size and local current relative proportion of Amazon mollies in the populations did not influence male preferences. We discuss potential causes for the variation of a sexual preference for conspecific females and how nondiscriminating male mating behavior can be adaptive in this complex.
Key words: coexistence, frequency dependency, gynogenesis, mate choice, Poeciliidae, seasonality, sex role, sexual selection.
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
|---|
Mating always takes place in a social and environmental context that may affect an individual’s sexual preferences. As this context changes over time, this may generate variability in the preferences measured in mate choice. Experimental studies on sexual preferences often overlook such variability in mate choice (Jennions and Petrie 1997
; Widemo and Saether 1999). Male mate choice and sexual preferences have been far less intensively studied than female mate choice. Nevertheless, conditions under which male mate choice can arise are defined (Bonduriansky 2001; Kokko and Monaghan 2001; Servedio and Lande 2006). Male mating decisions are important, especially when male parental investment increases and differences in female quality or offspring fitness occur, leading to situations with choosy males (Kraak and Bakker 1998; Berglund and Rosenqvist 2001; Gowaty et al. 2003; Wong and Jennions 2003; Herdman et al. 2004; Wong et al. 2005; Hoysak and Godin 2007) and strategic allocation of sperm (Reinhold et al. 2002; Wedell et al. 2002; Preston et al. 2003; Pound and Gage 2004; Byrne and Rice 2006; Ball and Parker 2007; Thomas and Simmons 2007; Riesch et al. 2008).
One system in which female quality varies greatly and male mate choice is important is in the context of the stability and maintenance of the asexual–sexual mating complex of the Amazon molly Poecilia formosa (Schlupp 2005; Schlupp and Plath 2005; Kokko et al. 2008; Riesch et al. 2008; Heubel KU, Rankin DJ, Kokko H, in preparation).
The asexual Amazon molly is an ovoviviparous all-female fish of the live-bearing family Poeciliidae (Hubbs CL and Hubbs LC 1932). It ameiotically produces offspring via gynogenesis, a special form of parthenogenesis, with a gestation period of 1 month. Hence, these asexually reproducing females rely on sperm of males from other closely related host species as a physiological stimulus to trigger embryogenesis (reviewed in Schlupp 2005). Sperm is normally not incorporated into the genome of the offspring (Schlupp et al. 1998). Therefore, Amazon mollies can be considered a sexual parasite of their sexual hosts with which they coexist in mixed populations. In South and Central Texas, USA, the sailfin molly, Poecilia latipinna, serves as the natural host species (Hubbs CL and Hubbs LC 1932; Darnell and Abramoff 1968; Schlupp et al. 1998, 2002).
Males should be choosy in this asexual–sexual mating complex because sailfin molly males have immediate costs and no direct benefit of mating with Amazon mollies. Mating with Amazon mollies might incur a cost of enhanced risk of predation (Farr 1975; Zuk and Kolluru 1998; Godin and McDonough 2003) and, while interacting and mating with Amazon mollies, males might miss opportunities to mate with conspecifics (Schlupp and Ryan 1996; Schlupp I, personal observation). Another cost of indiscriminately mating with both types of females depends on sperm availability. In Poeciliids, sperm is not an unlimited resource (Monaco et al. 1981; Pilastro and Bisazza 1999; Aspbury and Gabor 2004a, 2004b; Schlupp and Plath 2005; Riesch et al. 2008). Sperm depletion can be a problem for males in mixed asexual–sexual shoals of P. formosa and its sexual host species. Hubbs (1964) showed that Amazon mollies in South Texas were often partially pregnant and carried many unfertilized eggs in broods. He discussed that apparently skewed sex ratio and patterns of male mate selection led to unfertilized Amazon mollies. A similar pattern was reported by Riesch et al. (2008). An identical situation was also found in another complex of bisexual–unisexual fish species of Poeciliopsis (Poeciliidae) (McKay 1971; Moore and McKay 1971).
Consequently, theory predicts male preferences for conspecific sexual females (Clanton 1934; Kiester et al. 1981; Stenseth and Kirkendall 1985; Heubel KU, Rankin DJ, Kokko H, in preparation), but on the other hand, male preferences must not be as strong as one would assume at first glance (Moore and McKay 1971; Kiester et al. 1981; Kawecki 1988; Schmeller et al. 2005; Kokko et al. 2008; Heubel KU, Rankin DJ, Kokko H, in preparation). Schlupp et al. (1994) showed that mating with Amazon mollies may lead to an indirect benefit by increasing their chances of obtaining matings with conspecific females via heterospecific mate copying. In addition, Amazon mollies can be expected to show counteradaptations to thwart male choice, such as sexual mimicry (Schlupp et al. 1991; Lima et al. 1996; Dries 2003). Amazon mollies depend on matings with sperm-donating males in order to persist. Thus, in analogy to the "life/dinner principle" (Dawkins and Krebs 1979), selection on Amazon mollies to obtain matings may override selection on the males’ ability or effort to discriminate. Therefore, we cannot generally predict strong male preferences for conspecific females under all circumstances. It is rather likely to find males being more or less choosy depending on the specific circumstances and costs (Kokko and Monaghan 2001; Kokko and Johnstone 2002; Wong and Jennions 2003; Servedio and Lande 2006; Heubel KU, Rankin DJ, Kokko H, in preparation). Males might be choosier when mating is more costly due to sperm limitation, under high predation risk, absence of competition, locally high proportions of asexual females, lowered probability of benefiting from mate copying, and temporarily high chances of fathering offspring (Schlupp et al. 1994; Trexler et al. 1997; Simcox et al. 2005; Heubel et al. 2008; Plath et al. 2008; Riesch et al. 2008).
Assuming frequency-dependent behavioral plasticity in this mating complex, one would expect differences among populations and seasonal patterns of male sexual preferences. In populations with consistently very low proportions or absence of Amazon mollies, that is, allopatric populations or mixed allochthonous populations of very young sympatry (<150 generations) (Brown 1953; Drewry et al. 1958) and low frequency of Amazon mollies in Central Texas (Heubel 2004) males should be less discriminating than in autochthonous populations where sexual host species and Amazon mollies have been coexisting for more than 100,000 generations in South Texas (Avise et al. 1991; Schartl et al. 1995). Such reproductive character displacement has been shown in allopatric versus sympatric populations (Ryan et al. 1996; Gabor and Ryan 2001). Males from populations that are allopatric with P. formosa, or those from very recent sympatric populations, may be evolutionary "naive" and, as a consequence, less discriminating. By contrast, males originating from older sympatric populations are expected to discriminate more strongly between sexual and asexual females.
We predicted a seasonal pattern of mate choice discrimination with males exhibiting preferences for conspecific sexual females during peak reproductive periods, a few weeks before the number of juveniles peak in late spring (Hubbs 1964; Dries 2000), and less discriminative preferences for any type of female at other times of the year when reproduction ceases (e.g., in autumn) (Hubbs 1964). Alternatively, we considered frequency-dependent effects and tested whether the current proportion of asexuals present in the population had an effect on male preferences. In the present study on male sexual preferences, we directly take the individual's current natural context into account. Specifically, we addressed the question how seasonality and thus community ecology relates to the maintenance of sexual–asexual coexistence in this species complex. In this context, we emphasize the connection between seasonal variation in mixed populations on the one hand and male mating behavior and preferences on the other hand.
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
|---|
To examine the effects of season and frequency of Amazon mollies on male sailfin molly association preferences, we tested males with conspecific and heterospecific females in a simultaneous visual preference test. Male association time with female stimuli was measured.
Subjects
Fish were collected monthly a few (usually 5) days prior to testing at selected field sites in Texas, USA, in the wild between February and September 2001. Fish originated from mixed P. latipinna and P. formosa populations that have been regularly sampled in South (autochthonous) and Central Texas (allochthonous). We monitored population parameters such as sex ratio, adult size distribution, and relative proportion of juveniles (Figure 1) and unisexual females in the population. The populations were Comal Springs (COM) and San Marcos River (SM) in the Guadalupe River Basin in Central Texas and Weslaco North Floodway (WES) and Brownsville (BW) in the Nueces-Rio Grande River Basin in South Texas. A detailed description of field sites, population ecology, and sampling procedure are presented in Heubel (2004). From each population sampling visit, approximately every 25 days, up to 20 randomly selected adult males, females, and asexuals each were brought into the laboratory. All fish were maintained in 20- to 200-L tanks at 25–26 °C on a 12:12 h illumination cycle. All fishes were fed daily with commercially available flake food. After completing the experiments, all fish were released into large outdoor breeding tanks.
|
We separated species and sexes and allowed 5 days for individuals to acclimate to laboratory conditions before testing. Test males and stimulus females originated from the same population, whenever possible. However, males from COM (Witte and Ryan 2002
) were tested with adult female pairs of sailfin and Amazon mollies originating from the SM because COM is a population with extremely low relative densities of Amazon mollies (Table 1).
|
Test setup
A standard preference testing setup for simultaneous dual choice visual preference tests was used (Schlupp and Ryan 1996
; Landmann et al. 1999; Heubel and Schlupp 2006). The test tank (120 x 30 x 52 cm) was divided into 5 equal zones. The 2 outer compartments were separated from the 3 inner sections by clear Plexiglas dividers. The 3 inner zones were visually divided by vertically drawn pen markings at the front side of the tank. The central compartment was defined as a neutral zone. The test male was able to move freely among the 3 inner sections. The tank had a layer of gravel at the bottom, and illumination was provided directly from above by 2 fluorescent 40-W tubes, which emit visible light plus UV. The short ends and the rear long ends of the tank were covered with gray Teflon release sheet that reflects light of all wavelengths equally (Lunau K, personal communication). All dividers and the cylinder (10 x 10 cm) for acclimatization were made of UV translucent Plexiglas. The dividers were fitted tightly to reduce flow of water and chemical cues between the compartments. Water level and temperature in the test tank were stable during the experiment.
We measured standard length (SL) (snout to caudal peduncle) of females prior to testing to match size of stimuli and for males after testing (Table 1). We used only adult females with a body size of SL >28 mm to avoid inadvertent use of immature males instead of females as stimuli (Hubbs 1964).
Preference tests were initiated by introducing a test male into a clear cylinder in the center of the neutral zone. We always selected a size-matched conspecific sexual sailfin molly female and an asexual Amazon molly (mean size difference 0.2 ± 1.4 mm standard deviation). Both originated from the same population. These stimuli were introduced into randomly assigned outer stimulus compartments. After 5 min acclimatization, the cylinder was gently raised and the time the male spent in each of the 3 sections was recorded for 5 min (unit 1). Then the locations of the stimulus females were swapped, and the test was repeated immediately (unit 2) to control for a potential side bias. Males and females have only been used in one completed trial (units 1 and 2).
Statistical analysis and data handling
We analyzed the time spent with female stimuli in the 2 test units combined (before and after swapping sides to control for side bias). To compare male preferences seasonally and among populations, the relative time males spent with Amazon mollies was calculated as proportion of time the male spent in the compartment adjacent to the asexual female to the association time males spent with either female. For direct comparisons (Table 2), we used absolute times spent with females. It was a priori defined that a side bias occurred when a male spent more than 80% of its time on the same side of the tank before and after swapping side assignments of stimuli (Schlupp and Ryan 1996; Landmann et al. 1999). Those trials (n = 133) were excluded from further analysis. As an a priori set measure of male general responsiveness to the stimuli, we calculated the response index (RI), defined as the relative time males spent outside the neutral zone. Trials with males spending most of their time in the neutral zone in the center of the aquarium showing no response to any stimulus were terminated and excluded (n = 24) from further analysis (Schlupp et al. 1994; Schlüter et al. 1998; Landmann et al. 1999). The distribution of trial terminations due to side biases or low RIs was not significantly dependent on population origin (
2 = 3.517, degrees of freedom [df] = 3, P = 0.319, n = 255). However, the distribution of side biases fluctuated seasonally (2 = 18.063, df = 6, P = 0.006, n = 255).
|
In a general linear model (GLM), population origin of tested males and season were tested as factors and male size, current local relative proportion of unisexual females, and local relative proportion of juveniles in subsequent sampling month as covariates (Figure 1). We included the proportion of juveniles sampled during the next month because we were interested in potential patterns between male preferences and seasonal reproductive output in the studied populations. Because P. latipinna has an interbrood interval of approximately 35 days (Snelson et al. 1986
; Reznick and Miles 1989) and increased female receptivity after parturition (Parzefall 1973), we assumed that local reproduction is best represented by the number of juveniles collected at the field sites during each subsequent sampling visit in the following month. In a multiple regression GLM, we used relative time spent with Amazon mollies as response variable; population origin and season as categorical factors; and male size, proportion of unisexual females in population, and proportion of juveniles in the population during the following month as continuous factors.
Simultaneous choice tests were tested nonparametrically, and absolute association times were used. In a post hoc comparison, we compared pairwise mean differences of male's relative preference scores between different months within populations and applied Fisher's least significant difference tests.
When testing parametrically, proportions and relative time spent associated with one stimulus were arcsine transformed (Tabachnick and Fidell 2001). Graphical evaluation of probability plots revealed no severe divergence from normal distribution; thus, we relied on robustness of GLM (Quinn and Keough 2002). Data were analyzed using Systat 10 (SPSS 2000). All P values are 2 tailed.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
|---|
In a GLM with regular monthly sampling visits in 2001 (season) and population (COM vs. WES) as factors and male size as a covariate, season has a significant effect on male preference for females (F6,64 = 2.767, P = 0.019; Figure 2). There was no difference between populations (F1,64 = 0.000, P = 0.986), no significant interaction between spatial and temporal effects (F6,64 = 1.714, P = 0.132), and no effect of male body size (F1,64 = 2.236, P = 0.140). During late spring (defined as weeks 14–20, late March to mid-May; average ambient water temperature is 25 °C [other temperatures were winter: 19 °C, summer: 29 °C, and autumn: 27 °C]), males spent less time with heterospecific, gynogenetic sexual parasites (Figure 2).
|
Analyzing data on absolute male association times with conspecific sexual versus heterospecific asexual females for each sampling visit separately, there is a pattern of predominantly lacking male association preferences with conspecific females. Thus, in general, males did not show a preference for conspecific females (Table 2).
We analyzed all sampled and tested populations in a multiple regression GLM that tests for effects of all potential factors that may affect male mate preferences for conspecific sexual females versus unisexuals (Table 3). Whereas season has a significant effect (F6,84 = 2.358, P = 0.037), all other factors were nonsignificant (Table 3).
|
Comparing males’ behavior at different times of the season, males showed a nonsignificant tendency to spend more time with conspecific females in April (Wilcoxon test, n = 12, z = –1.65, P = 0.084) and a significant preference for conspecific females in May (Wilcoxon test, n = 8, z = –2.10, P = 0.036) (Figure 2). Males originating from WES again preferred to associate with sexual sailfin molly females in July (Sign test, n = 5, P < 0.04), whereas males from COM significantly preferred asexual Amazon mollies in March (Wilcoxon test: n = 6, z = –1.99, P = 0.046) (Figure 2).
We compared seasonal differences of male preference scores in post hoc pairwise comparisons. Males originating from COM showed preferences favoring the Amazon molly in March that were significantly different from the 3 subsequent months (Figure 2). Males originating from the WES population showed preferences favoring conspecific females in July that were significantly different from the previous and the following month (Figure 2).
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
|---|
We studied male association preferences in sailfin mollies and its relationship with season and frequency of Amazon mollies. In Poeciliids, visual association preferences are a suitable proxy measure for male mating preferences (Kodric-Brown 1993
; Plath et al. 2006). We found a seasonal variation in male mating preferences with males showing preferences for conspecific females during reproductive peaks of the season. Although a seasonality of female mate preferences has been reported in several taxa (e.g., Photinus fireflies: Cratsley and Lewis 2005; collared flycatchers: Qvarnström et al. 2000; sand gobies: Forsgren 1997), to our knowledge, this is the first study documenting seasonality of male mating preferences.
We did not detect a strong general preference for conspecific sexual females or a clear frequency-dependent pattern in male mate choice preferences or differences in male association time among populations. Whereas several other studies have found such preferences, there is an increasing number of studies that did not support preferences for conspecific sexual females in the unisexual–bisexual species complex of the Amazon molly (reviewed by Schlupp 2005). The lack of frequency-dependent preferences and no effect of male body size suggest that the maintenance of stable coexistence in this asexual–sexual mating complex cannot be explained by behavioral regulation sensu (McKay 1971; Moore and McKay 1971; Balsano et al. 1989). The behavioral regulation hypothesis was proposed to explain stability of the hybridogenetic asexual–sexual complexes in another group of live-bearing fish, Poeciliopsis (McKay 1971; Moore and McKay 1971). The authors suggested that males generally have a mating preference for conspecific females and that predominantly the subordinate males mate with asexual females. Such matings would be inversely proportional to the frequency of sexual females (Balsano et al. 1989). Dominance hierarchies that might lead to a similar pattern in the Amazon mollies mating system also exist among males of P. latipinna (Baird 1968) and Poecilia mexicana (Parzefall 1969; Balsano et al. 1985); however, in both species, these dominance hierarchies among males do not restrict access to females.
Males visually preferred conspecific females in spring (Figure 2)—approximately 1 month before the first cohort of juveniles were found in spring in standardized population samples in the field (Figure 1). Males from the southern population (WES) showed a second period of clear conspecific mate preference in July—again 1 month prior to another peak of numbers of juveniles in the population (Figure 1). Although it is not known which factor actually causes this relationship, it is an intriguing pattern. It shows, as predicted, that male choosiness varied seasonally. Males significantly preferred sexual females at times when being choosy were probably most beneficial.
Nevertheless, it is worth noting that Hubbs and Dries (2002) report much longer interbrood intervals (43–64 days) for both types of females originating from Texas if only stored sperm was used by the sexual and asexual females. They found a high variation among populations but no difference between species. It remains to be studied whether interbrood intervals also underlie seasonal variation.
In this sexual host–parasite system, asexuals might have evolved counteradaptations to host mate discrimination, rendering mate choice so costly (especially time consuming) that males sometimes will do better by indiscriminately mating with every female (Heubel KU, Rankin DJ, Kokko H, in preparation). Additionally, heterospecific and conspecific mate copying is well documented in this species complex (Schlupp et al. 1994; Witte and Ryan 2002; Heubel et al. 2008): males may become more attractive to conspecific females when interacting with Amazon mollies.
The present study focused only on male preferences based on visual cues to spatially associate with either type of females. How actual matings, sperm transfer, or mating success varies spatially, temporally, or dependent on the local frequency of Amazon mollies needs further investigation (Riesch et al. 2008). Male preferences for large females (Ptacek and Travis 1997; Gabor 1999) might be conflicting with a preference for conspecific females (Gumm and Gabor 2005), especially at times when the sexual parasite P. formosa is larger than sexual females. Males might have an underlying preference for conspecific females, but this can be countered by its even stronger preference for larger females at the end of the season (Heubel 2004).
More important than generalizing and speculating about presence and absence of sexual preferences across populations and season, it is relevant to investigate under which circumstances preferences do (or do not) occur. Expressing sexual preferences only during short but reproductively relevant bouts (of a population or individual), for example, as we show here, during seasonal reproductive peaks may be more efficient than maintaining a difficult and costly discrimination procedure throughout.
Our study clearly stresses one major result: there is a seasonal effect supporting the hypothesis of asynchronous initiation of reproductive activity, originally found in the P. mexicana–P. formosa complex (Monaco et al. 1978). The seasonal plasticity of male preferences indicates that male mating decisions are highly flexible and males might be able to consider carefully whether or not being choosy is beneficial under the given circumstances. This study also does not support that male size, current frequency of Amazon mollies, or different population origin per se might affect male mate preference patterns. Taking into account the predominating lack of a conspecific preference, this leads to the suggestion that it may not always pay for males to discriminate among potential mates.
|
FUNDING |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
|---|
The German Academic Exchange Service (DAAD HSPIII) (K.U.H.); Heisenberg fellowship of the Deutsche Forschungsgemeinschaft (DFG SCHL-344.7-1) to I.S; Academy of Finland to K.U.H.
|
ACKNOWLEDGEMENTS |
|---|
We thank A. Taebel-Hellwig, S.K. Repka, S. Keaton, N. Parvaze, and K. Chmielowiec for help conducting experiments, fieldwork, and fish care. We thank M.J. Ryan for providing facilities and his extensive support and encouragement during all stages of this study. We also thank Brackenridge Field Laboratory at the University of Texas at Austin for use of their outdoor facilities. Thanks to B. Wong and C. Gabor for discussion.
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
|---|
Aspbury AS, Gabor CR. Differential sperm priming by male sailfin mollies (Poecilia latipinna): effects of female and male size. Ethology (2004a) 110:193–202.[CrossRef][Web of Science]
Aspbury AS, Gabor CR. Discriminating males alter sperm production between species. Proc Natl Acad Sci USA (2004b) 101:15970–15973.
Avise JC, Trexler J, Travis J, Nelson WS. Poecilia mexicana is the recent female parent of the unisexual fish Poecilia formosa. Evolution (1991) 45:1530–1533.[CrossRef][Web of Science]
Baird RC. Aggressive behavior and social organization in Mollienesia latipinna Le Sueur. Tex J Sci (1968) 20:157–176.
Ball MA, Parker GA. Sperm competition games: the risk model can generate higher sperm allocation to virgin females. J Evol Biol (2007) 20:767–779.[CrossRef][Web of Science][Medline]
Balsano JS, Randle EJ, Rasch EM, Monaco PJ. Reproductive behavior and the maintenance of all-female Poecilia. Environ Biol Fishes (1985) 12:251–263.[CrossRef]
Balsano JS, Rasch EM, Monaco PJ. The evolutionary ecology of Poecilia formosa and its triploid associate. In: Ecology and evolution of livebearing fishes (Poeciliidae)—Meffe GK, Snelson FF, eds. (1989) Englewood Cliffs (NJ): Prentice Hall. 277–298.
Berglund A, Rosenqvist G. Male pipefish prefer ornamented females. Anim Behav (2001) 61:345–350.[CrossRef][Web of Science]
Bonduriansky R. The evolution of male mate choice in insects: a synthesis of ideas and evidence. Biol Rev (2001) 76:305–339.[Medline]
Brown WH. Introduced fish species of the Guadeloupe River Basin. Tex J Sci (1953) 5:245–251.
Byrne PG, Rice WR. Evidence for adaptive male mate choice in the fruit fly Drosophila melanogaster. Proc R Soc Lond B Biol Sci (2006) 273:917.[CrossRef][Medline]
Clanton W. An unusual situation in the salamander Ambystoma jeffersonianum. Occas Pap Mus Zool Univ Mich (1934) 290:1–14.
Cratsley CK, Lewis SM. Seasonal variation in mate choice of Photinus ignitus fireflies. Ethology (2005) 111:89–100.[CrossRef][Web of Science]
Darnell RM, Abramoff P. Distribution of the gynogenetic fish, Poecilia formosa, with remarks on the evolution of the species. Copeia (1968) 1968:354–361.[CrossRef]
Dawkins R, Krebs JR. Arms races between and within species. Proc R Soc Lond B Biol Sci (1979) 205:489–511.[Medline]
Drewry GE, Delco EA, Hubbs C. Occurence of the Amazon molly Mollienesia formosa at San Marcos, Texas. Tex J Sci (1958) 10:489–490.
Dries LA. The evolutionary persistence of the gynogenetic Amazon molly, Poecilia formosa (2000) Austin: University of Texas at Austin. [PhD thesis].
Dries LA. Peering through the looking glass at a sexual parasite: are Amazon mollies red queens? Evolution (2003) 57:1387–1396.[Web of Science][Medline]
Farr JA. The role of predation in the evolution of social behavior of natural populations of the guppy, Poecilia reticulata (Pisces: Poeciliidae). Evolution (1975) 29:151–158.[CrossRef][Web of Science]
Forsgren E. Mate sampling in a population of sand gobies. Anim Behav (1997) 53:267–276.[CrossRef][Web of Science]
Gabor C. Association patterns of Sailfin mollies (Poecilia latipinna): alternative hypotheses. Behav Ecol Sociobiol (1999) 46:333–340.[CrossRef][Web of Science]
Gabor CR, Ryan MJ. Geographical variation in reproductive character displacement in mate choice by male Sailfin mollies. Proc R Soc Lond B Biol Sci (2001) 268:1063–1070.[Medline]
Godin J-GJ, McDonough HE. Predator preference for brightly colored males in the guppy: a viability cost for a sexually selected trait. Behav Ecol (2003) 14:194–200.
Gowaty PA, Steinichen R, Anderson WW. Indiscriminate females and choosy males: within- and between-species variation in Drosophila. Evolution (2003) 57:2037–2045.[CrossRef][Web of Science][Medline]
Gumm JM, Gabor CR. Asexuals looking for sex: conflict between species and mate-quality recognition in Sailfin mollies (Poecilia latipinna). Behav Ecol Sociobiol (2005) 58:558–565.[CrossRef][Web of Science]
Herdman EJE, Kelly CD, Godin JGJ. Male mate choice in the guppy (Poecilia reticulata): do males prefer larger females as mates? Ethology (2004) 110:97–111.[CrossRef][Web of Science]
Heubel KU. Population ecology and sexual preferences in the mating complex of the unisexual Amazon molly Poecilia formosa (GIRARD, 1859) (2004) Hamburg (Germany): University of Hamburg. p. 1–137.
Heubel KU, Hornhardt K, Ollmann T, Parzefall J, Ryan MJ, Schlupp I. Geographic variation in female mate-copying in the species complex of a unisexual fish, Poecilia formosa. Behaviour (2008) 145:1041–1064.[CrossRef]
Heubel KU, Schlupp I. Turbidity affects association behaviour in male Poecilia latipinna. J Fish Biol (2006) 68:555–568.[CrossRef][Web of Science]
Hoysak DJ, Godin JGJ. Repeatability of male mate choice in the mosquitofish, Gambusia holbrooki. Ethology (2007) 113:1007–1018.[Web of Science]
Hubbs C. Interactions between bisexual fish species and its gynogenetic sexual parasite. Bull Tex Mem Mus (1964) 8:1–72.
Hubbs C, Dries LA. Geographic variation in interbrood interval in Poecilia. In: Libro Jubilar en Honor al Dr. Salvador Contreras Balderas—Lozano-Vilan ML, ed. (2002) Monterrey (Mexico): Universidad Autónoma de Nuevo Leon. 35–41.
Hubbs CL, Hubbs LC. Apparent parthenogenesis in nature in a form of fish of hybrid origin. Science (1932) 76:628–630.
Jennions MD, Petrie M. Variation in mate choice and mating preferences: a review of causes and consequences. Biol Rev Camb Philos Soc (1997) 72:283–327.[Medline]
Kawecki TJ. Unisexual/bisexual breeding complexes in Poeciliidae: why do males copulate with unisexual females? Evolution (1988) 42:1018–1023.[CrossRef][Web of Science]
Kiester AR, Nagylaki T, Shaffer B. Population dynamics of species with gynogenetic sibling species. Theor Popul Biol (1981) 19:358–369.[CrossRef][Web of Science]
Kodric-Brown A. Female choice of multiple male criteria in guppies: interacting effects of dominance, coloration and courtship. Behav Ecol Sociobiol (1993) 32:415–420.[Web of Science]
Kokko H, Heubel KU, Rankin DJ. How populations persist when asexuality requires sex: the spatial dynamics of coping with sperm parasites. Proc R Soc Lond B Biol Sci (2008) 275:817–825.[CrossRef][Medline]
Kokko H, Johnstone RA. Why is mutual mate choice not the norm? Operational sex ratios, sex roles and the evolution of sexually dimorphic and monomorphic signalling. Philos Trans R Soc Lond B Biol Sci (2002) 357:319–330.
Kokko H, Monaghan P. Predicting the direction of sexual selection. Ecol Lett (2001) 4:159–165.[CrossRef][Web of Science]
Kraak SBM, Bakker TCM. Mutual mate choice in sticklebacks: attractive males choose big females, which lay big eggs. Anim Behav (1998) 56:859–866.[CrossRef][Web of Science][Medline]
Landmann K, Parzefall J, Schlupp I. A sexual preference in the Amazon molly, Poecilia formosa. Environ Biol Fishes (1999) 56:325–331.[CrossRef]
Lima NRW, Kobak CJ, Vrijenhoek RC. Evolution of sexual mimicry in sperm-dependent all-female forms of Poeciliopsis (Pisces: Poeciliidae). J Evol Biol (1996) 9:185–203.[CrossRef][Web of Science]
McKay FE. Behavioral aspects of population dynamics in unisexual-bisexual Poeciliopsis (Pisces: Poeciliidae). Ecology (1971) 52:778–790.[CrossRef][Web of Science]
Monaco PJ, Rasch EM, Balsano JS. Cytological evidence for temporal differences during asynchronous ovarian maturation of bisexual and unisexual fishes of genus Poecilia. J Fish Biol (1978) 13:33–44.[CrossRef][Web of Science]
Monaco PJ, Rasch EM, Balsano JS. Sperm availability in naturally occurring bisexual-unisexual breeding complexes involving Poecilia mexicana and the gynogenetic teleost, Poecilia formosa. Environ Biol Fishes (1981) 6:159–166.[CrossRef]
Moore WS, McKay FE. Coexistence in unisexual-bisexual breeding complexes of Poeciliopsis (Pisces: Poeciliidae). Ecology (1971) 52:791–799.[CrossRef][Web of Science]
Parzefall J. Zur vergleichenden Ethologie verschiedener Mollienesia Arten einschliesslich einer Höhlenform von M. sphenops [German]. Behaviour (1969) 33:1–37.[Medline]
Parzefall J. Attraction and sexual cycle of Poeciliids. In: Genetics and mutagenesis of fish—Schröder JH, ed. (1973) Berlin (Germany): Springer. 177–183.
Pilastro A, Bisazza A. Insemination efficiency of two alternative male mating tactics in the guppy (Poecilia reticulata). Proc R Soc Lond B Biol Sci (1999) 266:1887–1891.[CrossRef]
Plath M, Blum D, Schlupp I, Tiedemann R. Audience effect alters mating preferences in a livebearing fish, the Atlantic molly, Poecilia mexicana. Anim Behav (2008) 75:21–29.[CrossRef][Web of Science]
Plath M, Seggel U, Burmeister H, Heubel KU, Schlupp I. Choosy males from the underground: male mating preferences in surface- and cave-dwelling Atlantic mollies (Poecilia mexicana). Naturwissenschaften (2006) 93:103–109.[CrossRef][Web of Science][Medline]
Pound N, Gage MJG. Prudent sperm allocation in Norway rats, Rattus norvegicus: a mammalian model of adaptive ejaculate adjustment. Anim Behav (2004) 68:819–823.[CrossRef][Web of Science]
Preston BT, Stevenson IR, Wilson K. Soay rams target reproductive activity towards promiscuous females’ optimal insemination period. Proc R Soc Lond B Biol Sci (2003) 270:2073–2078.[Medline]
Ptacek MB, Travis J. Mate choice in the sailfin molly, Poecilia latipinna. Evolution (1997) 51:1217–1231.[CrossRef][Web of Science]
Quinn GP, Keough MJ. Experimental design and data analysis for biologists (2002) Cambridge: Cambridge University Press.
Qvarnström A, Pärt T, Sheldon BC. Adaptive plasticity in mate preference linked to differences in reproductive effort. Nature (2000) 405:344–347.[CrossRef][Web of Science][Medline]
Reinhold K, Kurtz J, Engqvist L. Cryptic male choice: sperm allocation strategies when female quality varies. J Evol Biol (2002) 15:201–209.[CrossRef][Web of Science]
Reznick DN, Miles DB. A review of life history patterns in poeciliid fishes. In: Ecology and evolution of livebearing fishes (Poeciliidae)—Meffe GK, Snelson FF, eds. (1989) Englewood Cliffs (NJ): Prentice Hall. 125–148.
Riesch R, Schlupp I, Plath M. Female sperm limitation in natural populations of a sexual/asexual mating-complex (Poecilia latipinna, P. formosa). Biol Lett (2008) 4:266–269.
Ryan MJ, Dries LA, Batra P, Hillis DM. Male mate preferences in a gynogenetic species complex of Amazon mollies. Anim Behav (1996) 52:1225–1236.[CrossRef][Web of Science]
Schartl M, Wilde B, Schlupp I, Parzefall J. Evolutionary origin of a parthenoform, the Amazon molly Poecilia formosa, on the basis of a molecular genealogy. Evolution (1995) 49:827–835.[CrossRef][Web of Science]
Schlupp I. The evolutionary ecology of gynogenesis. Annu Rev Ecol Evol Syst (2005) 36:399–417.[CrossRef]
Schlupp I, Marler C, Ryan MJ. Benefit to male Sailfin mollies of mating with heterospecific females. Science (1994) 263:373–374.
Schlupp I, Nanda I, Döbler M, Lamatsch DK, Epplen JT, Parzefall J, Schmid M, Schartl M. Dispensable and indispensable genes in an ameiotic fish, the Amazon molly Poecilia formosa. Cytogenet Cell Genet (1998) 80:193–198.[CrossRef][Web of Science][Medline]
Schlupp I, Parzefall J, Schartl M. Male mate choice in mixed bisexual/unisexual breeding complexes of Poecilia (Teleostei: Poeciliidae). Ethology (1991) 88:215–222.[Web of Science]
Schlupp I, Parzefall J, Schartl M. Biogeography of the Amazon molly, Poecilia formosa. J Biogeogr (2002) 29:1–6.[CrossRef]
Schlupp I, Plath M. Male mate choice and sperm allocation in a sexual/asexual mating complex of Poecilia (Poeciliidae, Teleostei). Biol Lett (2005) 1:169–171.
Schlupp I, Ryan MJ. Mixed-species shoals and the maintenance of a sexual-asexual mating system in mollies. Anim Behav (1996) 52:885–890.[CrossRef][Web of Science]
Schlüter A, Parzefall J, Schlupp I. Female preference for symmetrical vertical bars in male Sailfin mollies. Anim Behav (1998) 56:147–153.[CrossRef][Web of Science][Medline]
Schmeller DS, O'Hara R, Kokko H. Male adaptive stupidity: male mating pattern in hybridogenetic frogs. Evol Ecol Res (2005) 7:1039–1050.
Servedio MR, Lande R. Population genetic models of male and mutual mate choice. Evolution (2006) 60:674–685.[Web of Science][Medline]
Simcox H, Colegrave N, Heenan A, Howard C, Braithwaite VA. Context-dependent male mating preferences for unfamiliar females. Anim Behav (2005) 70:1429–1437.[CrossRef][Web of Science]
Snelson FF, Wetherington JD, Large HL. The relationship between interbrood interval and yolk loading in a generalized poeciliid fish, Poecilia latipinna. Copeia (1986) 1986:295–304.[CrossRef]
Stenseth NC, Kirkendall LR. On the evolution of pseudogamy. Evolution (1985) 39:294–307.[CrossRef][Web of Science]
Tabachnick BG, Fidell LS. Using multivariate statistics (2001) 4th ed. Boston: Allyn and Bacon.
Thomas ML, Simmons LW. Male crickets adjust the viability of their sperm in response to female mating status. Am Nat (2007) 170:190–195.[CrossRef][Web of Science][Medline]
Trexler JC, Travis J, Dinep A. Variation among populations of the sailfin molly in the rate of concurrent multiple paternity and its implications for mating-system evolution. Behav Ecol Sociobiol (1997) 40:297–305.[CrossRef][Web of Science]
Wedell N, Gage MJG, Parker GA. Sperm competition, male prudence and sperm-limited females. Trends Ecol Evol (2002) 17:313–320.[CrossRef]
Widemo F, Saether SA. Beauty is in the eye of the beholder: causes and consequences of variation in mating preferences. Trends Ecol Evol (1999) 14:26–31.[CrossRef][Medline]
Witte K, Ryan MJ. Mate choice copying in the Sailfin molly, Poecilia latipinna, in the wild. Anim Behav (2002) 63:943–949.[CrossRef][Web of Science]
Wong BBM, Fisher HS, Rosenthal GG. Species recognition by male swordtails via chemical cues. Behav Ecol (2005) 16:818–822.
Wong BBM, Jennions MD. Costs influence male mate choice in a freshwater fish. Proc R Soc Lond B Biol Sci (2003) 270:S36–S38.[CrossRef]
Zuk M, Kolluru GR. Exploitation of sexual signals by predators and parasitoids. Q Rev Biol (1998) 73:415–438.[CrossRef]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  R. N.C. Milner, T. Detto, M. D. Jennions, and P. R.Y. Backwell Experimental evidence for a seasonal shift in the strength of a female mating preference Behav. Ecol., January 18, 2010; (2010) arp196v1. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. B. M. Wong and M. McCarthy Prudent male mate choice under perceived sperm competition risk in the eastern mosquito fish Behav. Ecol., March 1, 2009; 20(2): 278 - 282. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||