Digit ratio varies with sex, egg order and strength of mate preference in zebra finches

The steroid environment encountered by developing vertebrates has important organizational effects on physiology and behaviour that persist throughout an organism's lifetime. Optimal allocation of maternal steroids to zygotes may be difficult to achieve because of the sexually antagonistic effects of steroids; thus, for example, a hormone environment beneficial to a developing male may be much less beneficial to a developing female. Research into the important topic of how mothers might adaptively adjust steroid titres experienced by particular young has been constrained by the difficulty of measuring the steroid environment experienced by the embryo at critical times in development. A potential approach to this problem has been suggested by research on variation in digit ratios in humans, where the ratio of the length of the second and fourth digits reflects the steroid environment experienced by the foetus; notably, digit 4 lengthens in response to androgens. In light of the conservative nature of homeobox genes regulating early development in tetrapods, we questioned whether a sex difference in digit ratio exists in a passerine bird, the zebra finch, Taeniopygia guttata castanotis, and whether observed variation in the ratio is consistent with the previously reported pattern that androgen allocation to zebra finch egg yolk declines across laying order. We established an aviary population of outbred, wild-type zebra finches, and allowed them to breed freely. Hatchlings were marked to correspond to their egg order, and their digit ratios were measured after birds reached adulthood. We found that digit ratio increased across egg order, which is consistent with a pattern of decreasing androgen allocation. Moreover, digit ratios differed between the sexes. We also investigated whether variation in digit ratio among adult females predicted variation in their performance in mate-choice tests. Digit ratio accounted for almost 50% of the variance in strength of female preference for an attractive male trait: specifically, females with higher (presumably less 'androgenized') ratios had stronger preferences for attractive males. Digit ratio may prove to be an extremely useful tool for addressing a wide range of questions about vertebrate differentiation and behaviour.     

Resource allocation across the egg laying sequence in the wild zebra finch Taeniopygia guttata

Zebra finches have played a central role in the discovery of a variety of maternal effects over the past decade, with females shown to adjust resource allocation to their eggs in response to variables such as the appearance of their partner, their own condition, and the diet on which they are maintained. In addition to being the focus of some of the most high profile individual studies that have influenced maternal effects research in birds, the multitude of zebra finch studies together provide the most comprehensive set of data to illuminate general patterns and compare different maternally derived variables. Surprisingly, to date, virtually all of this work has focused on captive populations of the zebra finch that have been domesticated for many generations, and which are typically held under relatively constant environmental and dietary conditions. Here we report the first data on resource allocation across the egg laying sequence in a free‐living wild population. Reassuringly we find that the patterns that have been found in the majority of studies of domesticated populations with respect to investment across the laying sequence were all present in the wild population. The size and mass of eggs increased through the laying sequence whilst the concentration of carotenoids significantly decreased across the laying sequence. Although there was no significant pattern with respect to testosterone across the laying sequence the first two eggs had a higher level of testosterone than the last few eggs in the clutch, which is also consistent with the findings of earlier studies in captive populations.     

When mothers make sons sexy: maternal effects contribute to the increased sexual attractiveness of extra-pair offspring

Quality differences between offspring sired by the social and by an extra-pair partner are usually assumed to have a genetic basis, reflecting genetic benefits of female extra-pair mate choice. In the zebra finch (Taeniopygia guttata), we identified a colour ornament that is under sexual selection and appears to have a heritable basis. Hence, by engaging in extra-pair copulations with highly ornamented males, females could, in theory, obtain genes for increased offspring attractiveness. Indeed, sons sired by extra-pair partners had larger ornaments, seemingly supporting the genetic benefit hypothesis. Yet, when comparing ornament size of the social and extra-pair partners, there was no difference. Hence, the observed differences most likely had an environmental basis, mediated, for example, via differential maternal investment of resources into the eggs fertilized by extra-pair and social partners. Such maternal effects may (at least partly) be mediated by egg size, which we found to be associated with mean ornament expression in sons. Our results are consistent with the idea that maternal effects can shape sexual selection by altering the genotype-phenotype relationship for ornamentation. They also caution against automatically attributing greater offspring attractiveness or viability to an extra-pair mate's superior genetic quality, as without controlling for differential maternal investment we may significantly overestimate the role of genetic benefits in the evolution of extra-pair mating behaviour.     

Maternal effects influence the sexual behavior of sons and daughters in the zebra finch

Individual differences in sexual behavior have received much attention by evolutionary biologists, but relatively little is known about the proximate causes of this variation. We studied the quantitative genetics of male and female sexual behavior of captive zebra finches and found surprisingly strong maternal effects (differing between individual mothers) on the aggressiveness and song rate of sons and on the daughters' mating preferences for these male traits. We also found that daughters differed in their choosiness during mate-choice experiments depending on whether they originated from eggs produced early or late within the laying sequence of a clutch. Because this effect of laying order occurred independently of hatching order in cross-fostered broods, it must have been caused by consistent within-mother variation in maternal effects transmitted through the egg. Our findings raise the question whether these maternal effects might represent strategic programming of offspring behavior in response to the environment experienced by mothers or whether they are merely nonadaptive byproducts of developmental processes.     

The influence of differences in social experience on the development of species recognition in zebra finch males

Zebra finch males were first raised by zebra finch parents and then placed in a group of Bengalese finches between the ages of 30 and 60 days. A higher number of aggressive as well as non-aggressive initiatives by Bengalese finches towards young zebra finch males during this period was correlated with a more Bengalese-finch-directed sexual preference when these males were given a choice between a zebra finch and a Bengalese finch female as adults. Experiments in which a zebra finch male was exposed to Bengalese finches behind a wire screen or to Bengalese finch models gave corresponding results. The study shows that, in contrast to earlier findings, zebra finch males raised by their parents for 31 days can still develop a preference for Bengalese finches. Short term changes in preference are discussed. The results indicate that the behaviour shown by stimulus birds in studies on ‘sexual imprinting’ is important for the development of sexual preferences.     

Genetic basis of variation in morphological and life-history traits of a wild population of pink salmon

Understanding the genetic basis of phenotypic variation is essential for predicting the direction and rate of phenotypic evolution. We estimated heritabilities and genetic correlations of morphological (fork length, pectoral and pelvic fin ray counts, and gill arch raker counts) and life-history (egg number and individual egg weight) traits of pink salmon (Oncorhynchus gorbuscha) from Likes Creek, Alaska, in order to characterize the genetic basis of phenotypic variation in this species. Families were created from wild-caught adults, raised to the fry stage in the lab, released into the wild, and caught as returning adults and assigned to families using microsatellite loci and a growth hormone locus. Morphological traits were all moderately to highly heritable, but egg number and egg weight were not heritable, suggesting that past selection has eliminated additive genetic variation in egg number and egg weight or that there is high environmental variance in these traits. Genetic correlations were similar for nonadjacent morphological traits and adjacent traits. Genetic correlations predicted phenotypic correlations fairly accurately, but some pairs of traits with low genetic correlations had high phenotypic correlations, and vice versa, emphasizing the need to use caution when using phenotypic correlations as indices of genetic correlations. This is one of only a handful of studies to estimate heritabilities and genetic correlations for a wild population.     

Evidence of Phenotypic and Genetic Relationships between Sociality,Emotional Reactivity and Production Traits in Japanese Quail

The social behavior of animals, which is partially controlled by genetics, is one of the factors involved in their adaptation to large breeding groups. To understand better the relationships between different social behaviors, fear behaviors and production traits, we analyzed the phenotypic and genetic correlations of these traits in Japanese quail by a second generation crossing of two lines divergently selected for their social reinstatement behavior. Analyses of results for 900 individuals showed that the phenotypic correlations between behavioral traits were low with the exception of significant correlations between sexual behavior and aggressive pecks both at phenotypic (0.51) and genetic (0.90) levels. Significant positive genetic correlations were observed between emotional reactivity toward a novel object and sexual (0.89) or aggressive (0.63) behaviors. The other genetic correlations were observed mainly between behavioral and production traits. Thus, the level of emotional reactivity, estimated by the duration of tonic immobility, was positively correlated with weight at 17 and 65 days of age (0.76 and 0.79, respectively) and with delayed egg laying onset (0.74). In contrast, a higher level of social reinstatement behavior was associated with an earlier egg laying onset (-0.71). In addition, a strong sexual motivation was correlated with an earlier laying onset (-0.68) and a higher number of eggs laid (0.82). A low level of emotional reactivity toward a novel object and also a higher aggressive behavior were genetically correlated with a higher number of eggs laid (0.61 and 0.58, respectively). These results bring new insights into the complex determinism of social and emotional reactivity behaviors in birds and their relationships with production traits. Furthermore, they highlight the need to combine animal welfare and production traits in selection programs by taking into account traits of sociability and emotional reactivity.     

Quantitative genetics of oviposition behaviour and interactions among oviposition traits in the sand cricket

We performed a quantitative genetic study of oviposition behaviours and oviposition traits in the sand cricket Gryllus firmus. Egg survival in crickets depends on the depth at which they are inserted into the soil with the ovipositor. We examined whether egg depth depends on ovipositor length alone, or on both morphological and behavioural traits associated with oviposition. Heritability estimates were high (h² >0.5) for ovipositor length and small (h²=0.2) for oviposition behaviours. Negative genetic correlations between ovipositor length and some behavioural traits (digging depth and the behavioural component of egg depth) indicated compensation between oviposition traits on egg depth. Because of behavioural compensation, females with different ovipositor lengths subject to stabilizing selection on egg depth could have equal fitnesses. Females laid their eggs deeper, and their eggs were marginally more evenly distributed in dry than in wet sand. This suggests adaptive phenotypic plasticity in laying behaviour, but may also result from physical constraints of the substrate on the insertion of the ovipositor. The absence of significant between-family variation in oviposition traits in response to sand moisture indicates low evolutionary potential for phenotypic plasticity in oviposition traits according to soil moisture. In highly unpredictable environments, females could spread the risk of desiccation by laying eggs at different depths independently of environmental conditions (bet hedging). Our results show significant additive genetic influences on the ability of a female to spread risks as measured by genetic variation in egg distribution, suggesting that a bet-hedging strategy of egg laying has the potential to evolve in this population. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Basal metabolic rate can evolve independently of morphological and behavioural traits

Quantitative genetic analyses of basal metabolic rate (BMR) can inform us about the evolvability of the trait by providing estimates of heritability, and also of genetic correlations with other traits that may constrain the ability of BMR to respond to selection. Here, we studied a captive population of zebra finches (Taeniopygia guttata) in which selection lines for male courtship rate have been established. We measure BMR in these lines to see whether selection on male sexual activity would change BMR as a potentially correlated trait. We find that the genetic correlation between courtship rate and BMR is practically zero, indicating that the two traits can evolve independently of each other. Interestingly, we find that the heritability of BMR in our population (h²=0.45) is markedly higher than was previously reported for a captive zebra finch population from Norway. A comparison of the two studies shows that additive genetic variance in BMR has been largely depleted in the Norwegian population, especially the genetic variance in BMR that is independent of body mass. In our population, the slope of BMR increase with body mass differs not only between the sexes but also between the six selection lines, which we tentatively attribute to genetic drift and/or founder effects being strong in small populations. Our study therefore highlights two things. First, the evolvability of BMR may be less constrained by genetic correlations and lack of independent genetic variation than previously described. Second, genetic drift in small populations can rapidly lead to different evolvabilities across populations.     

Internal incubation and early hatching in brood parasitic birds

The offspring of brood parasitic birds benefit from hatching earlier than host young. A proposed but little-known strategy to achieve this is 'internal incubation', by retaining the egg in the oviduct for an additional 24 h. To test this, we quantified the stage of embryo development at laying in four brood parasitic birds (European cuckoo, Cuculus canorus; African cuckoo, Cuculus gularis; greater honeyguide, Indicator indicator; and the cuckoo finch, Anomalospiza imberbis). For the two cuckoos and the honeyguide, all of which lay at 48 h intervals, embryos were at a relatively advanced stage at laying; but for the cuckoo finch (laying interval: 24 h) embryo stage was similar to all other passerines laying at 24 h intervals. The stage of embryo development in the two cuckoos and honeyguide was similar to that of a non-parasitic species that lay at an interval of 44-46 h, but also to the eggs of the zebra finch Taeniopygia guttata incubated artificially at body temperature immediately after laying, for a further 24 h. Comparison with the zebra finch shows that internal incubation in the two cuckoos and honeyguide advances hatching by 31 h, a figure consistent with the difference between the expected and the observed duration of incubation in the European cuckoo predicted from egg mass. Rather than being a specific adaptation to brood parasitism, internal incubation is a direct consequence of a protracted interval between ovulation (and fertilization) and laying, but because it results in early hatching may have predisposed certain species to become brood parasitic.     

Variation in eggshell traits between geographically distant populations of pied flycatchers Ficedula hypoleuca

The expression and impact of maternal effects may vary greatly between populations and environments. However, little is known about large‐scale geographical patterns of variation in maternal deposition to eggs. In birds, as in other oviparous animals, the outermost maternal component of an egg is the shell, which protects the embryo, provides essential mineral resources and allows its interaction with the environment in the form of gas exchange. In this study, we explored variation of eggshell traits (mass, thickness, pore density and pigmentation) across 15 pied flycatcher populations at a large geographic scale. We found significant between‐population variation in all eggshell traits, except in pore density, suggesting spatial variation in their adaptive benefits or in the females’ physiological limitations during egg laying. Between‐ population variation in shell structure was not due to geographic location (latitude and longitude) or habitat type. However, eggshells were thicker in populations that experienced higher ambient temperature during egg laying. This could be a result of maternal resource allocation to the shell being constrained under low temperatures or of an adaptation to reduce egg water loss under high temperatures. We also found that eggshell colour intensity was positively associated with biliverdin pigment concentration, shell thickness and pore density. To conclude, our findings reveal large‐ scale between‐population variation of eggshell traits, although we found little environmental dependency in their expression. Our findings call for further studies that explore other environmental factors (e.g. calcium availability and pollution levels) and social factors like sexual selection intensity that may account for differences in shell structure between populations.     

The evolution of sexual size dimorphism in the house finch. V. Maternal effects

The phenotype of a mother and the environment that she provides might differentially affect the phenotypes of her sons and daughters, leading to change in sexual size dimorphism. Whereas these maternal effects should evolve to accommodate the adaptations of both the maternal and offspring generations, the mechanisms by which this is accomplished are rarely known. In birds, females adjust the onset of incubation (coincident with the first egg or after all eggs are laid) in response to the environment during breeding, and thus, indirectly, determine the duration of offspring growth. In the two house finch (Carpodacus mexicanus) populations that breed at the extremes of the species' distribution (Montana and Alabama), females experience highly distinct climatic conditions during nesting. We show that in close association with these conditions, females adjusted jointly the onset of incubation and the sequence in which they produced male and female eggs and consequently modified the growth of sons and daughters. The onset of incubation in newly breeding females closely tracked ambient temperature in a pattern consistent with the maintenance of egg viability. Because of the very different climates in Montana and Alabama, females in these populations showed the opposite patterns of seasonal change in incubation onset and the opposite sex bias in egg-laying order. In females with breeding experience, incubation onset and sex bias in laying order were closely linked regardless of the climatic variation. In nests in which incubation began with the onset of egg laying, the first-laid eggs were mostly females in Montana, but mostly males in Alabama. Because in both populations, male, but not female, embryos grew faster when exposed to longer incubation, the sex-bias produced highly divergent sizes of male and female juveniles between the populations. Overall, the compensatory interaction between the onset of incubation and the sex-biased laying order achieved a compromise between maternal and offspring adaptations and contributed to rapid morphological divergence in sexual dimorphism between populations of the house finch breeding at the climatic extremes of the species range.     

Parental and first generation effects of exogenous 17beta-estradiol on reproductive performance of female zebra finches (Taeniopygia guttata)

Steroids hormones have numerous "activational" effects in adult birds, regulating sexual behavior, and more recently maternal androgens have been shown to have potentially important "organizational" effects in ovo, influencing offspring growth, development, and behavior. In this study I investigated parental and first-generation effects of exogenous estrogens on female reproduction in zebra finches (Taeniopygia guttata). 17beta-Estradiol (E2; 1.2 microg/g, 4 daily injections i.m.) elevated plasma levels of the yolk precursors, vitellogenin (VTG) and very low-density lipoprotein (VLDL), in nonbreeding females to levels similar to those of breeding females. However, E2-treatment of breeding females caused no significant change in plasma VTG or VLDL levels compared to control birds (measured at the 1-egg stage), and there was no difference in reproductive performance between groups (egg size, clutch size, timing of laying). E2-treated females produced significantly more daughters than sons (21F:8M) at fledging, compared to control females (18F:19M). Nestling mortality was significantly higher in broods of E2-treated females, suggesting that the skewed sex ratio may have resulted from differential mortality of male chicks. The pattern of chick mortality in E2-broods was not consistent with this being caused by estrogen-mediated changes in parental behavior (e.g., provisoning). Mean egg mass of daughters of E2-treated females was typical of experienced, adult breeders, and larger than normal, first-time breeders or control offspring (0.947 vs 0.850 g). There was no treatment effect on offspring clutch size or laying interval. These results suggest that early exposure to maternal estrogens in ovo might be involved in establishing intraindividual variation in female-specific phenotypic traits, as has previously been demonstrated for androgens and male behavioral traits (e.g., aggression).     

Subtle manipulation of egg sex ratio in birds

Mothers are predicted to overproduce male or female eggs when the relative fitness gains from one sex are higher and outweigh the costs of manipulation. However, in birds such biases are often difficult to distinguish from differential embryo or chick mortality. Using a molecular technique to identify the sex of early embryos, we aim to determine the effect of maternal nutrition on zebra finch (Taeniopygia guttata) egg sex ratios after 2 days of incubation, which is as close to conception as is currently possible. We found no overall bias in the sex ratio of eggs laid and sex did not differ with relative laying order under any diet regime. However, mothers on a low-quality diet did produce a female bias in small clutches and a slight male bias in large clutches. On a high-quality diet, mothers produced a male bias in small clutches and a female bias in large clutches. Those on a standard diet produced a roughly even sex ratio, irrespective of clutch size. These observed biases in egg sex are partly in line with predictions that, in this species, daughters suffer disproportionately from poor rearing conditions. Thus, when relatively malnourished, mothers should only rear daughters in small broods and vice versa. Sex-ratio patterns in this species therefore appear to be subtle.     

Protoporphyrin‐based eggshell pigmentation predicts hatching success and offspring sex ratio in the barn swallow

Inter‐ and intraspecific variation in eggshell colouration has long fascinated evolutionary biologists. Among species, such variation may accomplish different functions, the most obvious of which is camouflage and background matching. Within species, it has been proposed that inter‐female variation in eggshell pigmentation patterns can reflect egg, maternal or paternal traits and hence may provide cues to conspecifics about egg, maternal or paternal phenotypic quality. However, the relationship between protoporphyrin‐based eggshell pigmentation and egg or maternal/paternal traits appears to be highly variable among species. We investigated patterns of intraspecific variation in Eurasian barn swallow Hirundo r. rustica protoporphyrin‐based eggshell pigmentation, and analysed its association with egg and clutch characteristics, maternal/paternal phenotypic traits and parental feeding effort. Eggshell pigmentation pattern significantly varied between breeding colonies, was significantly repeatable in first clutches laid by the same females in different years (intraclass correlation coefficient ranging between 0.56 and 0.63), but it was not significantly associated with egg traits, such as position in the laying sequence, egg mass, yolk testosterone concentration and antioxidant capacity. It was weakly or non‐significantly associated with female and male traits (sexual ornaments), but females laying darker (higher pigment intensity) first clutches had higher hatching success, suggesting that eggshell pigment intensity may predict fitness. Male nestling feeding effort was not predicted by eggshell pigmentation. In addition, females with darker breast plumage colouration (a melanin‐based trait related to fitness) laid highly protoporphyrin‐covered eggs, suggesting the presence of a previously unappreciated link between protoporphyrin biosynthesis and plumage melanisation. Moreover, the proportion of male offspring increased in clutches originating from highly protoporphyrin‐covered eggs, suggesting that parents could acquire visual cues about their future brood sex composition before egg hatching. Our results support the idea that intraspecific signalling via eggshell pigmentation is a species‐specific rather than a general feature of avian taxa.     

Nucleotide Variation, Linkage Disequilibrium and Founder-Facilitated Speciation in Wild Populations of the Zebra Finch (Taeniopygia guttata)

The zebra finch has long been an important model system for the study of vocal learning, vocal production, and behavior. With the imminent sequencing of its genome, the zebra finch is now poised to become a model system for population genetics. Using a panel of 30 noncoding loci, we characterized patterns of polymorphism and divergence among wild zebra finch populations. Continental Australian populations displayed little population structure, exceptionally high levels of nucleotide diversity (π = 0.010), a rapid decay of linkage disequilibrium (LD), and a high population recombination rate (ρ ≈ 0.05), all of which suggest an open and fluid genomic background that could facilitate adaptive variation. By contrast, substantial divergence between the Australian and Lesser Sunda Island populations (K_ST = 0.193), reduced genetic diversity (π = 0.002), and higher levels of LD in the island population suggest a strong but relatively recent founder event, which may have contributed to speciation between these populations as envisioned under founder-effect speciation models. Consistent with this hypothesis, we find that under a simple quantitative genetic model both drift and selection could have contributed to the observed divergence in six quantitative traits. In both Australian and Lesser Sundas populations, diversity in Z-linked loci was significantly lower than in autosomal loci. Our analysis provides a quantitative framework for studying the role of selection and drift in shaping patterns of molecular evolution in the zebra finch genome.     

GENETIC AND SOCIAL INHERITANCE OF BODY AND EGG SIZE IN THE BARNACLE GOOSE (BRANTA LEUCOPSIS)

We present heritability estimates for final size of body traits and egg size as well as phenotypic and genetic correlations between body and egg traits in a recently established population of the barnacle goose (Branta leucopsis) in the Baltic area. Body traits as well as egg size were heritable and, hence, could respond evolutionarily to phenotypic selection. Genetic correlations between body size traits were significantly positive and of similar magnitude or higher than the corresponding phenotypic correlations. Heritability estimates for tarsus length obtained from full-sib analyses were higher than those obtained from midoffspring-midparent regressions, and this indicates common environment effects on siblings. Heritabilities for tarsus length obtained from midoffspring-mother regressions were significantly higher than estimates from midoffspring-father regressions. The results suggest that this discrepancy is not caused by maternal effects through egg size, nor by extra-pair fertilizations, but by a socially inherited foraging site fidelity in females.     

Maternal effects due to male attractiveness affect offspring development in the zebra finch

Maternal effects occur when offspring phenotype is influenced by environmental factors experienced by the mother. Mothers are predicted to invest differentially in offspring in ways that will maximize offspring fitness depending on the environment she expects them to encounter. Here, we test for maternal effects in response to mate attractiveness on offspring developmental traits in the zebra finch Taeniopygia guttata. We controlled for parental genetic quality by manipulating male attractiveness using coloured leg rings and by randomly assigning mating pairs. The potential confounding effect of differential nestling care was controlled for by cross-fostering clutches and by allowing for variance due to foster father attractiveness in general linear models. We found a difference in egg mass investment between attractiveness groups and, importantly, we found that all of the offspring traits we measured varied with the attractiveness of the father. This provides strong evidence for maternal effects in response to mate attractiveness. Furthermore, due to the experiment design, we can conclude that these effects were mediated by differential investment of egg resources and not due to genetic differences or differences in nestling care.     

Phenotypic and genetic variation in emergence and development time of a trimorphic damselfly

Although colour polymorphisms in adult organisms of many taxa are often adaptive in the context of sexual selection or predation, genetic correlations between colour and other phenotypic traits expressed early in ontogeny could also play an important role in polymorphic systems. We studied phenotypic and genetic variation in development time among female colour morphs in the polymorphic damselfly Ischnura elegans in the field and by raising larvae in a common laboratory environment. In the field, the three different female morphs emerged at different times. Among laboratory-raised families, we found evidence of a significant correlation between maternal morph and larval development time in both sexes. This suggests that the phenotypic correlation between morph and emergence time in the field has a parallel in a genetic correlation between maternal colour and offspring development time. Maternal colour morph frequencies could thus potentially change as correlated responses to selection on larval emergence dates. The similar genetic correlation in male offspring suggests that sex-limitation in this system is incomplete, which may lead to an ontogenetic sexual conflict between selection for early male emergence (protandry) and emergence times associated with maternal morph.