Evidence that pairing with genetically similar mates is maladaptive in a monogamous bird

Background  

Evidence of multiple genetic criteria of mate choice is accumulating in numerous taxa. In many species, females have been shown to pair with genetically dissimilar mates or with extra-pair partners that are more genetically compatible than their social mates, thereby increasing their offsprings' heterozygosity which often correlates with offspring fitness. While most studies have focused on genetically promiscuous species, few studies have addressed genetically monogamous species, in which mate choice tends to be mutual.     

Pairing context determines condition-dependence of song rate in a monogamous passerine bird

Condition-dependence of male ornaments is thought to provide honest signals on which females can base their sexual choice for genetic quality. Recent studies show that condition-dependence patterns can vary within populations. Although long-term association is thought to promote honest signalling, no study has explored the influence of pairing context on the condition-dependence of male ornaments. In this study, we assessed the influence of natural variation in body condition on song rate in zebra finches (Taeniopygia guttata) in three different situations: during short and long encounters with an unfamiliar female, and within heterosexual mated pairs. We found consistent individual differences in male directed and undirected song rate. Moreover, body condition had a positive effect on song rate in paired males. However, male song rate was not influenced by body condition during short or long encounters with unfamiliar females. Song rate appears to be an unreliable signal of condition to prospective females as even poor-condition birds can cheat and sing at a high rate. By contrast, paired females can reliably use song rate to assess their mate''s body condition, and possibly the genetic quality. We propose that species'' characteristics, such as mating system, should be systematically taken into account to generate relevant hypotheses about the evolution of condition-dependent male ornaments.     

Female mate guarding: no evidence in a socially monogamous species

To understand the behavioural aspects of sperm competition, the costs and benefits to both sexes should be considered. However, few studies have addressed the costs to females of their social mate engaging in extrapair copulations (EPCs). Measures of female mate guarding have concentrated on female solicitation and copulation; however, females may also control access to their mate by maintaining close proximity, as is common in males. I recorded the maintenance of pair proximity behaviour of an urban population of the socially monogamous European blackbird, Turdus merula, over three breeding seasons. There was no evidence that females guarded their mates to prevent them from engaging in EPCs, nor were there any effects of the potential quality indicators of age, body size or male bill colour on the intensity of mate guarding between individuals. The study adds to a small body of literature suggesting that female mate guarding may be found in (facultatively) polygynous species, but not in socially monogamous ones. Copyright 2000 The Association for the Study of Animal Behaviour.     

Long sperm fertilize more eggs in a bird

Sperm competition, in which the ejaculates of multiple males compete to fertilize a female''s ova, results in strong selection on sperm traits. Although sperm size and swimming velocity are known to independently affect fertilization success in certain species, exploring the relationship between sperm length, swimming velocity and fertilization success still remains a challenge. Here, we use the zebra finch (Taeniopygia guttata), where sperm size influences sperm swimming velocity, to determine the effect of sperm total length on fertilization success. Sperm competition experiments, in which pairs of males whose sperm differed only in length and swimming speed, revealed that males producing long sperm were more successful in terms of (i) the number of sperm reaching the ova and (ii) fertilizing those ova. Our results reveal that although sperm length is the main factor determining the outcome of sperm competition, complex interactions between male and female reproductive traits may also be important. The mechanisms underlying these interactions are poorly understood, but we suggest that differences in sperm storage and utilization by females may contribute to the outcome of sperm competition.     

Socially transmitted mate preferences in a monogamous bird: a non-genetic mechanism of sexual selection

There is increasing evidence that animals can acquire mate preferences through the use of public information, notably by observing (and copying) the mate preferences of others in the population. If females acquire preferences through social mechanisms, sexual selection could act very rapidly to spread the preference and drive elaboration of the preferred trait(s). Although there are reports of 'mate-choice copying' in polygynous species, there is no clear evidence for this process in monogamous species. Here, we investigated whether adult female zebra finches Taeniopygia guttata can socially acquire sexual preferences for individual males and, in a separate study, for a generalized trait (coloured leg bands) of males. In both studies, test females observed males in two simultaneous conditions: a ('chosen') mixed-sex situation in which a male was paired with a (model) female, and a ('unchosen') same-sex situation in which a male was paired with another male. In the first experiment, after two weeks of females observing males, test females significantly preferred individual males who had been paired with another female (i.e. chosen males). In the second experiment, test females significantly preferred novel males that were wearing the same leg band colour as the apparently chosen males. Our findings are consistent with the conclusion that female zebra finches' mate preferences are altered by public information. Our study implies that mate preferences can spread rapidly through populations by social mechanisms, affecting the strength of sexual selection in a monogamous species.     

The costs of female choice in a lekking bird

We investigated the costs of active female choice in sage grouse,Centrocercus urophasianus, a lekking species in which femalesmake repeated, lengthy visits to leks to assess males beforemating. Several potential costs were measured by monitoringchanges in hens' ranging behavior, time budgets, and encounterrates with predators when they visited leks. Two costs wereidentified: hens moved further per day and encountered goldeneagles, Aquila chrysaetos, more frequently when visiting leks.However, extra travel due to visiting leks increased predicteddaily energetic expenditure by only about 1%, and the risk ofpredation by golden eagles over a typical series of lek visits(compared to a single short visit for mating) was estimatedto reduce annual survival by <0.1%. Two other potential costswere not supported: visiting leks did not depress foraging timeor conflict with nest defense. These results indicate that anycosts of mate choice are slight and imply that even very smallbenefits could be sufficient to maintain female choice. We presentcalculations which suggest that increased offspring viabilitydue to choosing fitter males could balance predation costs evenif the heritability of fitness is low and if females identifyfitter males with only moderate accuracy. Despite recent emphasison the direct benefits of mate choice, we conclude that eitherindirect or direct benefits could provide a plausible solutionto the lek paradox.     

Female choice, male interference, and sperm precedence in the red-spotted newt

Darwin first identified female choice and male—male competitionas forms of sexual selection resulting in the evolution of conspicuoussexual dimorphism, but it has proven challenging to separatetheir effects. Their effects on sexual selection become evenmore complicated when sperm competition occurs because spermprecedence may be either a form of cryptic female choice ora form of male—male competition. We examined the effectsof tail height on male—male competition and female choiceusing the sexually dimorphic red-spotted newt (Notophthalmusviridescens viridescens). Experiment 1 examined whether maletail height influenced male mating success. Males with deeptails were more successful at mating with females than thosewith shallow tails. Successful, deep-tailed males also were bigger(snout-vent length; SVL) than unsuccessful, shallow-tailed males,but they did not vary in tail length or body condition. Of these,only tail height and tail length are sexually dimorphic traits.Experiment 2 tested the hypothesis that the differential successof males with deeper tails was due to female choice by examiningboth simultaneous female preference for association and sequentialfemale choice. We found no evidence of female choice. When maleswere not competing to mate with females, tail height did notinfluence male mating success. Successful males did not havedifferent SVL and tail lengths than unsuccessful males. Thus,tail height in male red-spotted newts appears to be an intrasexuallyselected secondary sexual characteristic. Experiment 3 usedpaternity exclusion analyses based on molecular genetic markersto examine the effect of sperm precedence on sperm competitionin doubly-mated females. Sperm precedence likely does not havea pervasive and consistent effect on fertilization success becausewe found evidence of first, last, and mixed sperm usage.     

Selection on sperm morphology under relaxed sperm competition in a wild passerine bird

Theories regarding the role of sexual selection on the evolution of sperm traits are based on an association between pre-copulatory (e.g. female preference) and post-copulatory (e.g. ejaculate quality) male reproductive traits. In tests of these hypotheses, sperm morphology has rarely been used, despite its high heritability and intra-individual consistency. We found evidence of selection for longer sperm through positive phenotypic associations between sperm size and the two major female preference traits in the pied flycatcher, Ficedula hypoleuca. Our results support the sexually selected sperm hypothesis in a species under low sperm competition and demonstrate that natural and pre-copulatory sexual selection forces should not be overlooked in studies of intraspecific sperm morphology evolution.     

Ecological, social, and genetic contingency of extrapair behavior in a socially monogamous bird

Extrapair mating strategies are common among socially monogamous birds, but vary widely across ecological and social contexts in which breeding occurs. This variation is thought to reflect a compromise between the direct costs of mates' extrapair behavior and indirect benefits of extrapair fertilizations (EPF) to offspring fitness. However, in most free-living populations, the complete spatial and temporal distribution of mating attempts, genetic characteristics of available mates, and their relative contribution to EPF strategies are difficult to assess. Here we examined prevalence of EPF in relation to breeding density, synchrony, and genetic variability of available mates in a wild population of house finches Carpodacus mexicanus where all breeding attempts are known and all offspring are genotyped. We found that 15% of 59 nests contained extra-pair offspring and 9% of 212 offspring were sired by extra-pair males. We show experimentally that paired males and females avoided EPF displays in the presence of their social partners, revealing direct selection against EPF behavior. However, at the population level, the occurrence of EPF did not vary with nests dispersion, initiation date, synchrony, or with distance between the nests of extrapair partners. Instead, the occurrence of EPF closely covaried with genetic relatedness of a pool of available mates and offspring of genetically dissimilar mating tended to be resistant to a novel pathogen. These results corroborate findings that, in this population, strong fitness benefits of EPF are specific to each individual, thus highlighting the ecological, social, and genetic contingency of costs and benefits of an individual's extrapair behaviors.     

Maintenance of sperm variation in a highly promiscuous wild bird

Postcopulatory sexual selection is an important force in the evolution of reproductive traits, including sperm morphology. In birds, sperm morphology is known to be highly heritable and largely condition-independent. Theory predicts, and recent comparative work corroborates, that strong selection in such traits reduces intraspecific phenotypic variation. Here we show that some variation can be maintained despite extreme promiscuity, as a result of opposing, copulation-role-specific selection forces. After controlling for known correlates of siring success in the superb fairy-wren (Malurus cyaneus), we found that (a) lifetime extra-pair paternity success was associated with sperm with a shorter flagellum and relatively large head, and (b) males whose sperm had a longer flagellum and a relatively smaller head achieved higher within-pair paternity. In this species extrapair copulations occur in the same morning, but preceding, pair copulations during a female's fertile period, suggesting that shorter and relatively larger-headed sperm are most successful in securing storage (defense), whereas the opposite phenotype might be better at outcompeting stored sperm (offense). Furthermore, since cuckolding ability is a major contributor to differential male reproductive output, stronger selection on defense sperm competition traits might explain the short sperm of malurids relative to other promiscuous passerines.     

Consequences of a female-biased sex-ratio in a socially monogamous bird: female-female pairs in the Roseate Tern Sterna dougallii

In the socially monogamous gulls and terns, female-biased sex ratios are sometimes revealed by the occurrence of ‘supernormal clutches’, which are usually attended by female-female pairs or other multi-female associations. We studied these phenomena in the endangered Roseate Tern Sterna dougallii at Bird Island, USA, from 1970 to 1995. DNA-techniques were used to sex breeding adults in 1992–94. Supernormal clutches (with three or four eggs) have comprised 1–7% of all Roseate Tern clutches at Bird Island since at least 1970, probably increasing in frequency since 1980. Supernormal clutches were spatially clustered; most were laid late in the peak period of nesting during each season. More than 80% of supernormal clutches and at least 7% of normal clutches were attended by multi-female associations; most of these were female-female pairs, with a few trios (male + two females, or three females) and one quartet (four females). More than half of the multi-female associations attended normal clutches. Some female-female pairs were maintained for up to five years. The age-distribution of females mated to females did not differ significantly from that of females mated to males. Females mated together usually laid eggs synchronously (±2 days). Such females laid fewer eggs than females mated to males (means 1.20 versus 1.73), and had lower fertility and hatching success (about 46% versus 98%); they were less successful in raising young from eggs that did hatch (means 58% versus 73%), but this difference was not significant. Their overall breeding success was much lower (about 0.34 fledglings per female versus 1.35). The sex-ratio of breeders was about 127 females to 100 males; about 20% of breeding females did not have male mates. Female Roseate Terns that do not obtain male mates appear to be of low phenotypic ‘quality’ - based on late laying, small clutches and small eggs. Our data support the hypothesis that such females have a higher fitness if they mate with each other and raise a few young than if they do not breed at all.     

Mate choice in the monogamous and polychromatic Midas cichlid, Cichlasoma citrinellum

Choice of mate in the Midas cichlid, Cichlasoma citrinellum (Günther, 1864), has been examined from a number of perspectives, proceeding from general species attributes to individual differences.
The Midas cichlid discriminates against closely-related, highly-similar Cichlasoma , and recognizes sex, probably chemically in both cases. It is polychromatic and changes from the normal (N) pattern to gold (G) or even white at almost any age. Gold colouration inhibited attack and made it difficult to mate an N female with a G male; the inhibiting effect was cancelled by using a larger N female.
Because the Midas cichlid is also biparentally monogamous, early experience could easily influence later choice of mate. G females of G × G parents preferentially spawned adjacent to G males; N females of N × N spawned mainly before N males. N females of G × G pairs, however, showed no preference.
Groups of females were reared by all four combinations of two colours and two sexes, or by no parents. Females reared by identically pure-coloured parents responded most to males of those colours, whereas females raised by mixed-colour parents did not discriminate. Females reared without parents preferred N males. Regardless of their own or their parents' colour, juveniles spent more time with N juveniles and behaved less aggressively towards them, compared to G juveniles.
Fish were offered a choice among potential mates that differed in aggressiveness, size or breeding experience. Males did not choose on the basis of those traits. Females preferred large, aggressive, experienced males. Pairs with large aggressive males more readily kept a breeding territory, and aggressive experienced males guarded young more effectively. All females were equally aggressive in protecting their young.     

Female sperm storage in amphibians.

The three orders of extant amphibians are Gymnophiona, Anura, and Urodela. Although all gymnophionans apparently have internal fertilization and many are viviparous, female sperm storage is unknown. Internal fertilization has convergently evolved in a few anurans, but females of just one species, Ascaphus truei, are known to possess oviductal sperm storage tubules (SSTs). The SSTs of A. truei are similar anatomically to such glands in squamate reptiles. This similarity is convergence due to similar functional adaptations and/or internal design constraints. In salamanders and newts (Urodela), absence of sperm storage in females is the ancestral condition (three families). In the derived condition, sperm storage occurs in cloacal glands called spermathecae, and their possession is a synapomorphy for females in the suborder Salamandroidea (seven families). Salamandroids are the only vertebrates with cloacal sperm storage glands. In this paper, a phenetic analysis of variation in spermathecal characters reveals patterns of convergence in certain spermathecal characters in unrelated taxa that breed in similar habitats. In the family Salamandridae, a role in sperm nutrition for the spermathecal epithelium is questioned, and the widespread occurrence of spermiophagy is related to other reproductive strategies. I propose how the packaging of sperm in structurally different types of spermathecae may influence male paternity.     

Female sperm storage in reptiles.

Internal fertilization and oviparity most likely are symplesiomorphies for modern reptiles, and viviparity has evolved independently numerous times in Sauria and Serpentes. Oviducal sperm storage is known in females of all taxa except Amphisbaenia. However, in Rhynchocephalia and Crocodilia, sperm storage is poorly studied, and specialized sperm storage tubules (Ssts) are unknown. We use the molecular phylogenetic hypothesis [(Chelonia+Archosauria) (Squamata)] to trace evolution of sperm storage characters. Ssts arose independently in Chelonia and Squamata. Turtles possess albumen-secreting glands in the anterior half of the oviduct (the tuba or isthmus), and the most distal of these glands also serve as Ssts; in addition, some turtles possess Ssts in the adjacent segment of the oviduct, the uterus. Squamates lack albumen-secreting glands, and the ancestral state is possession of Ssts in the posterior infundibulum (uterine tube). Secondarily, iguanids have evolved vaginal Ssts. In this paper, we present the first ultrastructural observations on vaginal Ssts in lizards, using Anolis sagrei (Polychrotidae). Proximally, the neck of these simple tubular glands continues the alternation of ciliated and secretory cells lining the lumen of the vagina. However, the epithelial cells of the distal sperm storage area are neither secretory nor ciliated. The Ssts of Anolis are more similar to those of birds more than to infundibular receptacles in snakes and lizards.     

Predation risk determines breeding territory choice in a Mediterranean cavity-nesting bird community

Non-direct effects of predation can be an important component of the total effect of predation, modulating animal population and community dynamics. The isolated effects of predation risk on the spatial organisation of the breeding bird community, however, remains poorly studied. We investigated whether an experimentally increased predation risk prior to reproduction affected breeding territory selection and subsequent reproductive strategies in three Mediterranean cavity-nesting birds, i.e., the little owl Athene noctua, European roller Coracias garrulus and scops owl Otus scops. We found that territories used the previous year were more likely to be re-occupied when they belonged to the safe treatment rather than to the risky treatment. The first choice of breeders of all three species was for safe territories over risky ones. When all breeding attempts in the season (i.e., final occupation) were considered, breeders also preferred safe to risky sites. In addition, little owls laid larger eggs in risky territories than in safe territories. Our study provides experimental evidence of a rapid preventive response of the three most abundant species in a cavity-nesting bird community to a short-term manipulation of predation risk. This response highlights the key role of the non-direct effects of predation in modulating avian community organisation.     

Female mate choice as a condition-dependent life-history trait

The acquisition of resources is an important determinant of patterns of variation in and covariation among traits that are costly to produce and are dependent on condition for their expression. However, the extent to which variation in female mate choice behavior is condition dependent, and how this is related to other life-history traits, remains largely unknown. We manipulated the acquisition of dietary protein in the black field cricket, Teleogryllus commodus, and measured the effects of this on several important life-history traits and on female mate choice behavior. Females reared on a high-protein diet developed faster, were heavier at eclosion, and lived longer than females reared on a low-protein diet. Two lines of evidence suggest that female mate choice behavior in T. commodus is condition dependent. First, females reared on the high-protein diet were more sexually responsive and expressed stronger linear and quadratic preference functions for call rate and dominant frequency, respectively. Second, within treatments, females that developed faster were lighter, generally less sexually responsive, and, in the high-protein-diet treatment, expressed weaker preferences than slower-developing females. Collectively, our findings suggest an important role for resource acquisition in generating variation in mate choice behavior.