Influence of alternate reproductive tactics and pre- and postcopulatory sexual selection on paternity and offspring performance in a lizard

Sexual selection theory predicts different optima for multiple mating in males and females. We used mating experiments and genetic paternity testing to disentangle pre- and postcopulatory mechanisms of sexual selection and alternate reproductive tactics in the highly promiscuous lizard Eulamprus heatwolei. Both sexes mated multiply: 30–60 % of clutches were sired by two to four fathers, depending on the experiment. Larger males sired more offspring when we allowed male contest competition: 52 % of large males but only 14 % of small males sired at least one offspring. In the absence of male contest competition, females mated promiscuously and there was no large male advantage: 80 % of large males and 90 % of small males sired at least one offspring, and there was no evidence for last-male precedence. Multiple mating did not yield obvious direct or indirect benefits to females. E. heatwolei represents a complex system in which males attempt to improve their fertility success by limiting rivals from access to females and through adopting alternate reproductive tactics. Conversely, females exhibit no obvious precopulatory mate choice but may influence fitness through postcopulatory means by either promoting sperm competition or through cryptic female choice. Our results support the hypothesis that female multiple mating in nonavian reptiles is best explained by the combined effect of mate encounter frequency and high benefits to males but low costs to females.     

The use of genetic markers to estimate the frequency of successful alternative reproductive tactics

Summary This paper outlines a method for estimating rates of successful alternative reproductive tactics from parental exclusions known through the use of genetic markers. We review a method for calculating the probability of excluding a putative father when he is not the actual father. We adapt this method to model two mating tactics of concern to sociobiologists: extrapair copulations (EPCs) and intra-specific egg parasitism (egg-dumping). Four different types of parental exclusions are possible (both male and female, male only, female only, and ambiguous). The two models predict different proportions of each type of exclusion. Models are also generated for the case when the putative mother's or father's genotypes are not available.We used parental exclusions from an electrophoretic study of indigo buntings (Westneat 1987b) to demonstrate these methods. The distribution of parental exclusions in the buntings departed significantly from the predictions of the egg-dumping model, but agreed well with those of the EPC model. The probability of detection for the EPC model (0.401) was then used to estimate the actual rate of extra-pair fertilizations (0.421 of all the young sampled). We present a method for calculating a confidence interval on this estimate, which ranged from 0.247 to 0.659. We concluded that these methods will allow the quantitative study of the success of alternative reproductive tactics in a wide variety of species.     

Alternative reproductive tactics in the spider Meta segmentata

Summary In the spider Meta segmentata web site quality and competitive ability determine female distributions, and ultimately male mating strategy. Large, fecund females position their webs in aggregations in high quality habitats, whereas small females live alone in lower quality sites. Competition for web sites is intense. Large females have a fighting advantage, but web ownership can offset size disadvantages of about 10%. Males compete for access to female webs. The smallest males are excluded from aggregations of females but have a very high probability of mating monogamously with females in poor habitats. The largest males move about within aggregations and by mating with many females achieve the highest reproductive gains. Moderately sized males only have a low probability of mating in an aggregation, but for those that do succeed the reproductive gains are higher than for those that mate monogamously in low quality areas. On average, moderately sized males obtain reproductive gains from the high risk, high gain strategy of defending webs in aggregations that are equal to those from definding solitary females in poor areas. That 18 of 21 moderately sized males defend females in aggregations suggests that M. segmentata behaves in a riskprone fashion.     

Evolution of extreme-mating behaviour: patterns of extrapair paternity in a species with forced extrapair copulation

Sexual conflict can result in the evolution of extreme mating strategies, including forced copulation. Forced extrapair copulation (FEPC) is generally rare among birds, but is common in re-introduced populations of the hihi (Notiomystis cincta), a socially monogamous, New Zealand endemic, endangered passerine. The aim of this study was to understand the patterns of extrapair paternity in a population where the majority of EPC is forced and to examine the factors, in particular female-specific, influencing the proportion of offspring fathered by extrapair males (EPP—extrapair paternity) and the number of males siring extrapair offspring within a brood (EPM) in this species. Using 8 years of comprehensive paternity, life-history and demographic information for 485 breeding attempts, we show that the frequency of EPP is dependent on (1) social male and female age, (2) the month the female fledged, (3) breeding density and (4) whether it was their first or second reproductive event of the season. In addition, we show that both EPP and EPM are negatively associated with breeding synchrony and clutch size is the most important predictor of EPM. Understanding the drivers of EPP and EPM in species with FECP is important because these are strong determinants of variance in reproductive success and the maintenance of extreme mating behaviour.     

Larval paternity and male reproductive success of a broadcast-spawning gorgonian, Plexaura kuna

Male reproductive success of the broadcast-spawning gorgonian, Plexaura kuna Lasker, Kim and Coffroth, 1996, was measured in June 1994 and June and July 1995 at two sites in the San Blas Islands, Panamá in order to determine the environmental and biotic factors affecting individual reproductive success. Developing embryos were collected in the field during natural spawning events, and paternity determined using randomly amplified polymorphic DNA markers. Analyses of F₁ progeny from defined laboratory matings established that the markers were inherited in Mendelian fashion, and allowed the determination of the zygosities of the markers. P. kuna is clonal, but male reproductive success was not strictly proportional to clone size. Proximity to females appeared to have a greater effect on male reproductive success than clone size, and on both reefs the most successful male clone was the one closest to the spawning female clone. Current direction and transport of gametes by eddies explained variation in paternity assignments between nights. Clonal propagation allows clones to grow and spread toward each other, and may enhance male reproductive success. Received: 1 April 1997 / Accepted: 11 February 1998     

Colony size,but not density,affects survival and mating success of alternative male reproductive tactics in a polyphenic mite,Rhizoglyphus echinopus

Among acarid mites, a number of species are characterised by the presence of discontinuous morphologies (armed heteromorphs vs. unarmed homeomorphs) associated with alternative mating tactics (fighting vs. scramble competition). In Rhizoglyphus echinopus, expression of the fighter morph is suppressed, via pheromones, in large, dense colonies. If this mechanism is adaptive, fighters should have relatively lower fitness in large and/or dense colonies, due to costs incurred from fighting, which is often fatal. In order to test these predictions, we quantified the survival and mating success of fighters and scramblers in colonies of equal sex and morph ratios; these colonies either differed in size (4, 8, or 32 individuals) but not density or differed in density but not size (all consisted of 8 individuals). We found that the relative survival and mating success of fighters was inversely related to colony size, but we did not find a significant effect of colony density. The higher mating success of fighters in small colonies was due to the fact that, after killing rival males, these fighters were able to monopolise females. This situation was not found in larger colonies, in which there was a larger number of competitors and fighters suffered relatively higher mortality. These results indicate that morph determination, guided by social cues, allows for the adaptive adjustment of mating tactics to existing demographic conditions.     

Sperm characteristics associated with different male reproductive tactics in bluegills (Lepomis macrochirus)

We examined the availability and motility of sperm from parental and sneaker male bluegills (Lepomis macrochirus), a colonially nesting sunfish (Family Centrarchidae) with male parental care and a high incidence of cuckoldry by both sneaker and satellite males. We found no differences between sneakers and parentals in length and swimming speed of sperm, or percent and duration of sperm activity. In sneaker milt, however, sperm was almost 50% more concentrated than in parental milt (16.5×10⁶ vs 11.5×10⁶ sperm/μl of milt, respectively). Despite this difference in sperm concentration, stripped ejaculates from sneakers contained almost 400 million fewer sperm (only 32% as many sperm) than those from parentals due to their much smaller stripped ejaculate volumes (only about 19% that of parentals). Thus unless sneakers can compensate by releasing more sperm or gaining closer proximity to eggs at the time of spawning, they may be at a disadvantage with respect to sperm competition. We discuss these results in relation to models for the evolution of alternative reproductive behaviours in this species and suggest that the cuckolders may be making the best of a bad situation. Received: 18 February 2000 / Revised: 23 March 2000 / Accepted: 14 September 2000     

Male reproductive tactics to increase paternity in the polygynandrous Columbian ground squirrel (<Emphasis Type="Italic">Urocitellus columbianus</Emphasis>)

In polyandrous and polygynandrous species where females mate with multiple partners, males are expected to maximize their fitness by exhibiting an array of reproductive behaviors to ensure fertilization success, such as competing for the best mating order within a mating sequence, optimizing their investment in copulation, and mate guarding. Though there is genetic evidence of a first-male precedence in siring success for many mammalian species, the causes of this effect are poorly understood. We studied influences on first-male precedence in Columbian ground squirrels (Urocitellus columbianus). We found that the time a male spent consorting and mate guarding declined with his mating order (both the highest for the first male to mate). Mate guarding by the first male significantly reduced, but did not exclude, the number of additional males a female accepted. Later mating males reduced the time spent consorting, suggesting a perceived decreased chance of fertilization success. Consortship and mate guarding durations were positively related to the male’s siring success and to each other, suggesting that males adjusted these behaviors strategically to increase their chances of fertilization success. Our results suggest that besides being the first male to consort, first-male sperm precedence is further enhanced through longer mating bouts and by suppressing the chances and/or efforts of later mating males.     

Cuckoldry rates in the Molly Miller (<Emphasis Type="Italic">scartella cristata</Emphasis>; blenniidae), a hole-nesting marine fish with alternative reproductive tactics

Microsatellite markers were developed and employed to assess genetic maternity and paternity of embryos in nest-tended clutches of the Molly Miller (Scartella cristata), a marine fish in which alternative reproductive tactics (ARTs) by males were recently described from behavioral and morphological evidence. Genetic data gathered for 1,536 surveyed progeny, from 23 barnacle-nest holes in a single Floridian population, indicate that on average about 5.5 females (range 3–9) contributed to the pool of progeny within a nest. With regard to paternity, the microsatellite data demonstrate that most of the surveyed nests (82.6%) contained at least some embryos that had not been sired by the nest-tending (bourgeois) male, and overall that 12.4% of offspring in the population had been sired via "stolen" fertilizations by other males. These are among the highest values of cuckoldry documented to date in nest-tending fishes, and they support and quantify the notion that the nest-parasitic ART is reproductively quite successful in this species despite what would otherwise seem to be highly defensible nesting sites (the restricted interior space of a barnacle shell). Our estimated cuckoldry rates in this population of the Molly Miller are compared to those previously reported for local populations in other nest-tending fish species, with results discussed in the context of ecological and behavioral variables that may influence relative frequencies of nest parasitism.     

Sex-specific reproductive behaviours and paternity in free-ranging Barbary macaques (Macaca sylvanus)

In a wide variety of species, male reproductive success is determined by contest for access to females. Among multi-male primate groups, however, factors in addition to male competitive ability may also influence paternity outcome, although their exact nature and force is still largely unclear. Here, we have investigated in a group of free-ranging Barbary macaques whether paternity is determined on the pre- or postcopulatory level and how male competitive ability and female direct mate choice during the female fertile phase are related to male reproductive success. Behavioural observations were combined with faecal hormone analysis for timing of the fertile phase (13 cycles, 8 females) and genetic paternity analysis (n = 12). During the fertile phase, complete monopolisation of females did not occur. Females were consorted for only 49% of observation time, and all females had ejaculatory copulations with several males. Thus, in all cases, paternity was determined on the postcopulatory level. More than 80% of infants were sired by high-ranking males, and this reproductive skew was related to both, male competitive ability and female direct mate choice as high-ranking males spent more time in consort with females than low-ranking males, and females solicited copulations mainly from dominant males. As most ejaculatory copulations were female-initiated, female direct mate choice appeared to have the highest impact on male reproductive success. However, female preference was not directly translated into paternity, as fathers were not preferred over non-fathers in terms of solicitation, consortship and mating behaviour. Collectively, our data show that in the Barbary macaque, both sexes significantly influence male mating success, but that sperm of several males generally compete within the female reproductive tract and that therefore paternity is determined by mechanisms operating at the postcopulatory level.     

Impacts of environmental heterogeneity on alternative mating tactics in the threadtail damselfly

Environmental heterogeneity, including variation in the physical environment, may be key to understanding the evolution and maintenance of alternative mating tactics, but its influence is rarely examined. Males of the threadtail damselfly Protoneura amatoria reversibly use two alternative mating tactics (perching vs. hovering) and have previously been found to modulate their use of these tactics in response to variation in both light conditions and the density of ovipositing females. Here, I show that mating success payoffs of the two tactics are differentially influenced by these factors. The payoff of the perching tactic was greater than that of the hovering tactic under low light conditions and at low densities of ovipositing females. The payoff of the hovering tactic was greater under high light conditions and higher densities of ovipositing females. The differential success of the two mating tactics in response to light conditions is discussed in light of flight dynamics, vision, and predation.     

Alternative male mating tactics in a cichlid, Pelvicachromis pulcher: a comparison of reproductive effort and success

Pelvicachromis pulcher is a small African cichlid which breeds in holes. Males may either reproduce monogamously (pair males), polygynously (harem males), or be tolerated as helpers in a harem territory (satellite males). These helpers share in defence of the territory against conspecifics, heterospecific competitors and predators. There are two male colour morphs that are fixed for life and are apparently genetically determined. These differ in their potential mating strategy. Red morph males may become harem owners, while yellow morph males may become satellite males, and males of both morphs may alternatively pair up monogamously. We compared the reproductive effort and success of these three male reproductive strategies. Effort was measured as attack rates, time expenditure and the risk of being injured or killed when attacking competitors or predators of three sympatric fish species. Reproductive success was measured by observing how many eggs were fertilized by each male when this was possible, and by using genetic markers. The number of fry surviving to independence of parental care was used as a criterion of success. The reproductive success of harem males was 3.3 times higher than that of pair males and 7 times higher than that of the average satellite male. Dominant satellite males, however, were as successful as monogamous pair males, using the measure of fertilized eggs. To our knowledge, this has not been found previously in any fish species. Both harem and pair males had lower parental defence costs per sired offspring, however, than males using the alternative satellite tactic. Defence effort was significantly related to the risk of injury. Received: 17 January 1996 / Accepted after revision: 9 June 1997     

Male reproductive success: paternity contribution to queens and workers in Formica ants

The relative number of workers and female sexuals fathered by two males mated with a queen were directly assessed using microsatellite and allozyme markers in field colonies of the ants Formica exsecta and F. truncorum. In both species one of the two males consistently fathered more offspring than the other. There was, however, no evidence that one male might be particularly successful in fathering a disproportionally high proportion of female sexuals relative to the proportion of workers. Moreover, in F. exsecta, the proportions of worker pupae and worker adults fathered by each male did not differ significantly between cohorts. The most likely explanation for this pattern is that females store different amounts of sperm from the two males they mated with. Received: 10 January 1997 / Accepted after revision: 22 March 1997     

Sperm traits in the quacking frog (<Emphasis Type="Italic">Crinia georgiana</Emphasis>), a species with plastic alternative mating tactics

In species where males use alternative reproductive tactics and male phenotypes are confronted with different risks of sperm competition, theory predicts that between-male-type differences in sperm expenditure may evolve. In the frog Crinia georgiana big males can monopolize females, whereas small males often engage in polyandrous matings. Consequently, big males may experience a lower risk of sperm competition than do small males. We tested if the predictions from theoretical models can be applied to the mating system of C. georgiana. Our results showed that small males do not have larger testes relative to their body size compared to their larger counterparts and that the efficiency with which sperm number, size, motility, and longevity are produced by the testes does not differ between small and large males in the predicted way. These results are not in alignment with predictions from a loaded raffle model of sperm competition on sperm expenditure in males with alternative phenotypes. The plasticity in mating tactics used by C. georgiana males and a high intraseasonal variation in male densities may have prevented the evolution of enhanced sperm performance in smaller males. A fair raffle in the sperm competition game played by C. georgiana males could also explain the observed patterns in sperm traits. Future investigations determining the parameters responsible for the deviation from theoretical predictions in this system will test the degree to which current theoretical models can indeed be applied to species with plastic reproductive tactics.     

Testing a post-copulatory pre-zygotic reproductive barrier in a passerine species pair

Sexual selection may drive speciation, but most research focuses on pre-copulatory sexual selection, overlooking post-copulatory processes. Post-copulatory sexual selection in allopatric populations could drive divergence in post-copulatory pre-zygotic (PCPZ) phenotypes, limiting gene flow upon secondary contact. Here, we performed in vitro experiments examining one potential PCPZ barrier between two closely related passerine species, house sparrows (Passer domesticus) and Spanish sparrows (Passer hispaniolensis). In birds, crossing in the vagina may be particularly challenging for sperm, so we tested the effect of female reproductive tract fluids on sperm swimming speed and motility. If a PCPZ barrier exists at this stage of the fertilization process, heterospecific female fluids are predicted to reduce sperm swimming speed or motility relative to conspecific female fluid. We found that house sparrow female fluids affected the two species’ sperm asymmetrically, depending on the control sperm velocity and male species. Overall, however, sperm performed equally in conspecific and heterospecific female fluids, and the species had similar sperm morphology and sperm swimming performance. Low divergence in PCPZ phenotypes between species, perhaps because post-copulatory sexual selection is stabilizing or only moderately strong in these taxa, may be insufficient to cause an overall PCPZ barrier. Reinforcement may be unlikely to drive PCPZ barriers for this species pair, because relatively effective pre-copulatory barriers exist between the species, and because hybrids can be quite successful. Testing the role of PCPZ barriers in birds with more divergent PCPZ phenotypes will improve our understanding of speciation in passerines.     

Displaying in the dark: light-dependent alternative mating tactics in the Alpine newt

Environment plays a major role for determining the kind of courtship behaviours or alternative mating tactics employed, but the effect of physical variables on fitness has received little attention. The Alpine newt courts during both day and night times and exhibits a complex suite of behaviours involving olfactory, visual and tactile cues. Displaying in both dark and light conditions may increase the number of mating opportunities and alleviate predation risk, but the frequency and efficacy of the various tactics deployed may vary across light conditions, leading males to vary their use of these tactics across different light regimes. To test this hypothesis, we video-recorded sexual encounters at two light intensities in a controlled experimental design. When courting in the dark, males used comparatively more olfactory rather than visual displays. They also relied more on positive feedback from the female before releasing a spermatophore for her to pick up. The particular mix of tactics used under each light condition is likely to be adaptive because in the dark (1) visual communication is hampered, making olfactory displays possibly more effective and (2) males depositing spermatophores are more likely to lose fertilizations to competitors. Mating in light and dark conditions has similar reproductive payoffs, which shows that displaying in the dark is not detrimental and may even be advantageous if predation risk is reduced at night. These results confirm the importance of taking into account physical variables to understand the evolution of sexual communication in animals.     

Singing activity stimulates partner reproductive investment rather than increasing paternity success in zebra finches

Song is used as a signal in sexual selection in a wide range of taxa. In birds, males of many species continue to sing after pair formation. It has been suggested that a high song output after pair formation might serve to attract extra-pair females and to minimise their own partner’s interest in extra-pair copulations. A non-exclusive alternative function that has received only scant attention is that the amount of song might stimulate the own female’s investment into eggs in a quantitative way. We address these hypotheses in a captive population of zebra finches, Taeniopygia guttata, by relating male undirected song output (i.e. non-courtship song) to male egg siring success and female reproductive investment in two different set-ups. When allowed to breed in aviaries, males with the highest song output were no more attractive than others to females in an analysis of 4,294 extra-pair courtships involving 164 different males, and they also did not sire more offspring (both trends were against the expectation). When breeding in cages with two different partners subsequently, females produced larger eggs with more orange yolks when paired to a male with a high song output. These findings suggest that singing activity in paired zebra finch males might primarily function to stimulate the partner and not to attract extra-pair females.     

High degree of multiple paternity in the viviparous Shiner Perch, <Emphasis Type="Italic">Cymatogaster aggregata</Emphasis>, a fish with long-term female sperm storage

The Shiner Perch (Cymatogaster aggregata Gibbons) exhibits a viviparous reproductive mode and long-term female sperm storage, two biological features that may predispose this fish species for both intense sperm competition and frequent multiple paternity within broods. To test these hypotheses, we used polymorphic microsatellite markers to identify sires and quantify paternal contributions to the progeny arrays of 27 pregnant females from a natural population of C. aggregata. The number of sires per brood ranged from one to eight (mean 4.6), typically with skewed distributions of fertilization success by the fathers but no correlation between sire number and brood size. The extraordinarily high incidences of multiple paternity in this species probably are due in part to high rates of mate encounter, but selection pressures related to the avoidance of maternal–fetal incompatibility may further have promoted the evolution of polyandrous mating behaviors in this female-pregnant species. Our genetic data are consistent with the hypothesis that viviparity, long-term sperm storage, and extreme polyandry are interrelated reproductive phenomena that should promote the evolution of post-copulatory sperm competition and/or cryptic female choice in these fishes.