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Quantitative genetics research in Zebra Finches: Where we are and where to go
Abstract
The ease with which Zebra Finches can be kept and bred in captivity makes them a suitable model for avian quantitative genetic studies. After a brief introduction to some quantitative genetic concepts, we here provide an up-to-date overview of quantitative genetic studies in Zebra Finches. We discuss what these studies can teach us about the evolutionary and behavioural ecology of Zebra Finches and song birds in general, and make suggestions for future research. Throughout this article we plead for a greater appreciation of the advantages offered by working on captive birds, but also discuss their limitations. Although quantitative genetic analyses in natural populations are becoming increasingly powerful, these studies lack the control possible in captivity. However, obtaining meaningful estimates of the type and strength of selection acting on phenotypic variation is more difficult in captivity. Hence, quantitative genetic studies in the wild and captivity each have their strengths and weaknesses and should be considered complementary rather than opposing. However, whereas quantitative genetic studies in the wild have boomed, the unique advantages offered by captive Zebra Finches have remained underexploited. Here we make a first attempt at changing this by highlighting what we believe may be fruitful lines for future research.
... Zebra finches are commonly used in laboratory and field studies [50,51]. Their genome has been fully sequenced [52] and the ease with which they can be bred and maintained in captivity has made them a model for studies of avian physiology, behavior, development, and evolution [53,50]. Zebra finches have recently emerged as a system for captive toxicological studies [3,22,[54][55][56][57][58][59][60][61]. ...
... Perhaps more convincingly, our data support a robust conclusion that there is substantial genetic variance to blood mercury levels in our captive zebra finches. Mean-scaled measures of additive genetic variation (CV A ) for the 0.6 and 1.2 ppm mercury dietary treatments exceeded CV A values reported for most physiological, ornamental, and morphological traits in a recent review of quantitative genetics in the zebra finch [53]. Overall, these results indicate that there is substantial genetic variation for factors that lead to sub-lethal accumulation of mercury in the blood of these birds when the birds are exposed to mercury levels that could occur at a contaminated site. ...
Mercury is a ubiquitous metal contaminant that negatively impacts reproduction of wildlife and has many other sub-lethal effects. Songbirds are sensitive bioindicators of mercury toxicity and may suffer population declines as a result of mercury pollution. Current predictions of mercury accumulation and biomagnification often overlook possible genetic variation in mercury uptake and elimination within species and the potential for evolution in affected populations. We conducted a study of dietary mercury exposure in a model songbird species, maintaining a breeding population of zebra finches (Taeniopygia guttata) on standardized diets ranging from 0.0-2.4 ?g/g methylmercury. We applied a quantitative genetics approach to examine patterns of variation and heritability of mercury accumulation within dietary treatments using a method of mixed effects modeling known as the 'animal model'. Significant variation in blood mercury accumulation existed within each treatment for birds exposed at the same dietary level; moreover, this variation was highly repeatable for individuals. We observed substantial genetic variation in blood mercury accumulation for birds exposed at intermediate dietary concentrations. Taken together, this is evidence that genetic variation for factors affecting blood mercury accumulation could be acted on by selection. If similar heritability for mercury accumulation exists in wild populations, selection could result in genetic differentiation for populations in contaminated locations, with possible consequences for mercury biomagnification in food webs.
... As the relative number of heritability estimates for life-history traits has increased over time (Figure 2.1b), this further contributed to the observed reduction in the mean heritability over time. Several studies have found that, across species, life-history traits have lower heritabilities than morphological traits (Mousseau & Roff 1987;Houle 1992;Tschirren & Postma 2010). Similarly, within populations and species, traits more closely related to fitness tend to have lower heritabilities (Gustafsson 1986;Merilä & Sheldon 2000;McCleery et al. 2004;Teplitsky et al. 2009). ...
... Indeed, life-history traits tend to have higher and morphological traits lower CV A s, both within (e.g. Merilä & Sheldon 2000;Coltman et al. 2005;Tschirren & Postma 2010) (but see McCleery et al. 2004;Teplitsky et al. 2009) and across species and populations (Houle 1992;this chapter). ...
This book gathers the expertise of thirty evolutionary biologists from around the globe to highlight how applying the field of quantitative genetics (the analysis of the genetic basis of complex traits) to wild populations has provided major advancements in evolutionary ecology. It offers insights into the relevant methods and major discoveries in a wide array of evolutionary fields, such as life-history theory, behavioural ecology, and sexual selection, as well as the most promising emerging topics including the application to non-model taxa such as plants and arthropods, molecular quantitative genetics, and non-additive genetic variance.
... Intergenerational effects do not only arise postnatally but also during the prenatal period. The estimation of such prenatal effects has, however, been hampered by the fact that they are not easily disentangled from additive genetic effects (Krist and Remeš 2004;Tschirren and Postma 2010;Pick, Ebneter, et al. 2016). Consequently, few studies have considered the long-term effects of differential prenatal investment, and even fewer the effect of the prenatal environment on the future reproductive performance of the offspring (Krist 2011). ...
Maternal effects are prevalent in nature and significantly contribute to variation in phenotypic trait expression. However, little attention has been paid to the factors shaping variation in the traits mediating these effects (maternal effectors). Specific maternal effectors are often not identified, and typically they are assumed to be inherited in an additive genetic and autosomal manner. Given that these effectors can cause long‐lasting effects on offspring phenotype, it is likely that they may also affect themselves in the next generation. Although the existence of such cascading maternal effects has been discussed and modeled, empirical examples of such effects are rare, let alone quantitative estimates of their strength and evolutionary consequences. Here, we demonstrate that the investment a mother makes in her eggs positively affects the egg investment of her daughters. Through reciprocally crossing artificially selected lines for divergent prenatal maternal investment in Japanese quail (Coturnix japonica), we demonstrate that the size of eggs daughters lay resembles the egg size of their maternal line significantly more than that of their paternal line, highlighting that egg size is in part maternally inherited. Correspondingly, we find that variation in the daughters' egg size is in part determined by maternal identity, in addition to substantial additive genetic effects. Furthermore, this maternal variance in offspring egg size is fully explained by maternal egg size, demonstrating the presence of a positive cascading effect of maternal egg size on offspring egg size. Finally, we use an evolutionary model to quantify the consequences of covariance between cascading maternal and additive genetic effects for both maternal effector and offspring body mass evolution. Our study demonstrates that by amplifying the amount of variation available for selection to act on, positive cascading maternal effects can significantly enhance the evolutionary potential of maternal effectors and the offspring traits that they affect.
... Intergenerational effects do not only arise postnatally but also during the prenatal period. The estimation of such prenatal effects has, however, been hampered by the fact that they are not easily disentangled from additive genetic effects (Krist and Remeš 2004;Tschirren and Postma 2010;Pick, Ebneter, et al. 2016). Consequently, few studies have considered the long-term effects of differential prenatal investment, and even fewer the effect of the prenatal environment on the future reproductive performance of the offspring (Krist 2011). ...
Maternal effects are prevalent in nature and significantly contribute to variation in phenotypic trait expression. However, little attention has been paid to the factors shaping variation in the traits mediating these effects (maternal effectors). Specific maternal effectors are often not identified, and typically they are assumed to be autosomally inherited. Given that these effectors can cause long-lasting effects on offspring phenotype, it is likely that they may also affect themselves in the next generation. Although the existence of such cascading maternal effects has been discussed and modelled, empirical examples of such effects are rare, let alone quantitative estimates of their strength and evolutionary consequences. Here we demonstrate that the investment a mother makes in her eggs positively affects the egg investment of her daughters. Through reciprocally crossing artificially selected lines for divergent prenatal maternal investment, we demonstrate that the size of eggs daughters lay resembles the egg size of their maternal line significantly more than that of their paternal line, highlighting that egg size is in part maternally inherited. Correspondingly, we find that variation in the daughters' egg size is in part determined by maternal identity, in addition to substantial additive genetic effects. Furthermore, this maternal variance in offspring egg size is fully explained by maternal egg size, demonstrating the presence of a positive cascading effect of maternal egg size on offspring egg size. Finally, we use an evolutionary model to quantify the consequences of covariance between cascading maternal and additive genetic effects for both maternal effector and offspring body mass evolution. Our study demonstrates that, by amplifying the amount of variation available for selection to act on, positive cascading maternal effects can significantly enhance the evolutionary potential of maternal effectors and the offspring traits that they affect.
... As mothers provide their offspring with both genes and the developmental environment, maternal effects are prone to be confounded with direct additive genetic effects. Although exchanging offspring between families ('cross-fostering') can separate postnatal maternal effects from both prenatal and direct genetic effects, this experimental technique cannot remove the potential covariance between prenatal maternal effects and offspring genotype (additive genetic correlation), as cross-fostering would have to happen before prenatal maternal effects occur (Krist and Remeš 2004;Tschirren and Postma 2010;Wolf et al. 2011). The use of isogenic or inbred lines, along with an environmental manipulation would also allow additive genetic effects to be removed (e.g. ...
Organisational processes during prenatal development can have long-term effects on an indi- vidual’s phenotype. Because these early developmental stages are sensitive to environmental influences, mothers are in a unique position to alter their offspring’s phenotype by differentially allocating resource to their developing young. However, such prenatal maternal effects are diffi- cult to disentangle from other forms of parental care, additive genetic effects and/or other forms of maternal inheritance, hampering our understanding of their evolutionary consequences. Here we used divergent selection lines for high and low prenatal maternal investment, and their re- ciprocal line crosses, in a precocial bird, the Japanese quail (Coturnix japonica), to quantify the relative importance of genes and prenatal maternal effects in shaping offspring phenotype. Ma- ternal, but not paternal, origin strongly affected offspring body size and survival throughout development. Although the effects of maternal egg investment faded over time, they were large at key life stages. Additionally, there was evidence for other forms of maternal inheritance af- fecting offspring phenotype at later stages of development. Our study is among the first to successfully disentangle prenatal maternal effects from all other sources of confounding varia- tion and highlights the important role of prenatal maternal provisioning in shaping offspring traits closely linked to fitness.
... Similar quantitative genetic approaches have been applied to study the evolution of resistance to other ecotoxins [24], but there has been limited application to the evolution of mercury tolerance in vertebrates, and none in birds. There have also been studies of quantitative genetics of morphology and coloration in zebra finches [48,49], but at much smaller sizes than included in our large breeding design. ...
... Bolund et al. 2010). However, the limitations of the method are that it is an observational approach that provides little insight into the underlying mechanisms and causes of the maternal effects exposed (Tschirren and Postma 2010). ...
Birds are a particularly good group with which to examine the importance of maternal effects, as parental contributions can be relatively easily quantified compared with other groups. There have undoubtedly been more studies on maternal effects in the Zebra Finch than any other single bird species. Studies of this species have examined the importance of maternal effects mediated through sex allocation, size, nutrients and hormones of of eggs, incubation behaviour and provisioning levels. A synthesis of all of this work illustrates some contrasting results (e.g. many high-profile results have failed to be replicated), some very common patterns (e.g. investment shifts through the laying sequence), and potentially interesting and complex interactions between traits (e.g. between sex of offspring and hormonal profiles of eggs). This extensive collection of work on the Zebra Finch provides useful general insight into the patterns of maternal investment in birds and the effects on offspring phenotype. However, we caution that the literature is probably littered with studies that have overemphasised the importance of some maternal effects and recent studies have highlighted analytical and logical flaws that have probably led to misplaced confidence in some of the findings reported to date. Finally, it is worth considering that the bulk of the literature is based on studies of captive domesticated birds and ecological and physiological data from individuals in the wild is currently lacking. The biological relevance of maternal effects documented in this model species is therefore unclear.
... However, while controlling for potentially confounding factors that complicate studies in the wild may be beneficial in some circumstances, other questions can be better answered using study systems in the wild. For example, otherwise limiting resources become equally available in captivity, which [64] may in turn diminish (intrinsic) differences between individuals. The latter has to be taken into account when interpreting the results as obtained in captivity as biological meaningful insights into natural systems [65]. ...
Introduction
Maternal effects occur when the phenotype of the offspring is influenced by the phenotype of the mother, which in turn depends on her heritable state as well as on influences from the current and past environmental conditions. All of these pathways may, therefore, form significant sources of variation in maternal effects. Here, we focused on the maternal transfer of carotenoids and vitamin E to the egg yolk, using canaries as a model species. Maternal yolk carotenoids and vitamin E are known to generate significant phenotypic variation in offspring, representing examples of maternal effects. We studied the intra-individual consistency in deposition patterns across two years and the mother-daughter resemblance across two generations in order to estimate the level of heritable variation. The effects of the current environmental conditions were studied via a food supplementation experiment, while the consequences of past environmental conditions were estimated on the basis of the early growth trajectories.
Results
There was a significant effect of the current environmental conditions on the yolk carotenoid and vitamin E deposition, but this effect varied between antioxidant components. The deposition of yolk carotenoids and vitamin E were linked to the process of yolk formation. Past environmental conditions did not contribute to the variation in yolk carotenoid and vitamin E levels nor did we find significant heritable variation.
Conclusions
The transfer of carotenoids or vitamin E may be an example where current environmental variation is largely passed from the mother to the offspring, despite the numerous intermediate physiological steps that are involved. Differences in the effect of the environmental conditions as experienced by the mother during laying may be due to differences in availability as well as physiological processes such as competitive exclusion or selective absorption.
... All three beak dimensions show considerable additive genetic variance. The narrow-sense heritability estimates for beak depth and width are among the highest estimates for morphological traits in general and certainly for beak dimensions in avian species (Keller et al. 2001;Å kesson et al. 2008;Tschirren & Postma 2010). This might reflect the reduced environmental variation in the captive environment (but see the review of Weigensberg & Roff 1996 for sometimes higher heritability estimates in the wild as compared to the laboratory). ...
The intra- and interspecific diversity of avian beak morphologies is one of the most compelling examples for the power of natural selection acting on a morphological trait. The development and diversification of the beak have also become a textbook example for evolutionary developmental biology, and variation in expression levels of several genes is known to causally affect beak shape. However, until now, no genomic polymorphisms have been identified, which are related to beak morphology in birds. QTL mapping does reveal the location of causal polymorphisms, albeit with poor spatial resolution. Here, we estimate heritability and genetic correlations for beak length, depth and width and perform a QTL linkage analysis for these traits based on 1404 informative single-nucleotide polymorphisms genotyped in a four-generation pedigree of 992 captive zebra finches (Taeniopygia guttata). Beak size, relative to body size, was sexually dimorphic (larger in males). Heritability estimates ranged from 0.47 for beak length to 0.74 for beak width. QTL mapping revealed four to five regions of significant or suggestive genome-wide linkage for each of the three beak dimensions (nine different regions in total). Eight out of 11 genes known to influence beak morphology are located in these nine peak regions. Five QTL do not cover known candidates demonstrating that yet unknown genes or regulatory elements may influence beak morphology in the zebra finch.
... Studies on captive species are, therefore, likely to be valuable especially if traits are studied that are difficult to measure in the wild due to e.g. low recruitment rates [42]. The fact that the highest heritability estimates were obtained in the wild population may be due to the confounding effects of the early rearing conditions (see above) that were only partly controlled for in the wild [44]. ...
Maternal effects occur when the phenotype of the mother affects the phenotype of their offspring. They are thought to have evolved to translate the environmental conditions experienced by the mother into adaptive phenotypic variation of the offspring. However, the integration of environmental cues allowing adaptive responses requires some form of plasticity that depends on the interaction of the maternal phenotype and her environment. In birds, maternal yolk hormones represent such a pathway for maternal effects, and their adaptive significance depends thus on the plasticity in maternal yolk hormone deposition. We studied sources of variation in yolk testosterone deposition, focusing on the often neglected contribution of the (partly heritable) maternal phenotype. We investigated consistency and heritability of yolk testosterone deposition in captive canaries of which the F(1) generation was raised in foster nests and analyzed the potential effects of the early developmental conditions. We found significant female consistency across years in egg mass, yolk mass and total amount of yolk testosterone but not in yolk testosterone concentrations. Females varied the yolk testosterone concentrations of their eggs across years mainly via changes in yolk mass. The heritable variation in egg mass, yolk mass and amount of yolk testosterone but not yolk testosterone concentrations was within the range of previous studies, but not significantly different from zero. Finally, the growth of the daughters as nestling had a significant effect on their yolk testosterone deposition at adulthood indicating the transgenerational potential for environmental effects - via the effects of yolk hormones on offspring development.
Abstract Nutritional conditions during development can affect both structural growth and body fat deposition. Body size and body fat each have significant consequences for fitness, yet few studies have investigated how young birds balance resource allocation between structural growth and fat reserves. We raised zebra finches (Taeniopygia guttata) in consistently high- or low-food conditions until posthatch day 35 (PHD 35). From this age until PHD 62, half of the birds in each condition were switched to the other treatment, while the rest were maintained on the same conditions. Body mass, lean mass, body fat, and tarsus length were measured before (PHD 25) and after (PHD 55) nutritional independence. Precise measures of body composition were obtained noninvasively at both ages using quantitative magnetic resonance analysis. At PHD 25, birds in the high treatment had more body mass and lean mass than birds in the low treatment, but nutritional treatments did not affect body fat at this age. Unexpectedly, the strategic response of birds that experienced deteriorating food availability was to maintain body mass by increasing body fat and decreasing lean mass. Birds that experienced an improvement in food availability significantly increased body mass by increasing lean mass and not body fat. Birds maintained on a low diet throughout did not significantly increase body mass, lean mass, or body fat. Tarsus length was not affected by nutritional manipulations. These findings indicate that nutritional stress did not affect the relationship between skeletal growth and body fat deposition because lean mass, body fat, and tarsus length can be independently regulated at different developmental periods depending on nutritional conditions.
Birds are a particularly good group with which to examine the importance of maternal effects, as parental contributions can be relatively easily quantified compared with other groups. There have undoubtedly been more studies on maternal effects in the Zebra Finch than any other single bird species. Studies of this species have examined the importance of maternal effects mediated through sex allocation, size, nutrients and hormones of of eggs, incubation behaviour and provisioning levels. A synthesis of all of this work illustrates some contrasting results (e.g. many high-profile results have failed to be replicated), some very common patterns (e.g. investment shifts through the laying sequence), and potentially interesting and complex interactions between traits (e.g. between sex of offspring and hormonal profiles of eggs). This extensive collection of work on the Zebra Finch provides useful general insight into the patterns of maternal investment in birds and the effects on offspring phenotype. However, we caution that the literature is probably littered with studies that have overemphasised the importance of some maternal effects and recent studies have highlighted analytical and logical flaws that have probably led to misplaced confidence in some of the findings reported to date. Finally, it is worth considering that the bulk of the literature is based on studies of captive domesticated birds and ecological and physiological data from individuals in the wild is currently lacking. The biological relevance of maternal effects documented in this model species is therefore unclear.
Today,theZebra FinchisAustralia'smoststudiedbird andthefocus ofintensive multi-million dollar research projectsthroughouttheworld.HerewebrieflysummarisethehistoryoftheZebraFinchinscienceanddocumentthewayin whichstudiesofthisspecieshaveproliferatedanddominatedanumberofquitedifferent fieldswithinthebiologicalsciences. TheimportanceoftheZebraFinchislikelytoincreasestillfurtheraftertherecentpublicationofitsgenomesequence-only thesecondbirdtobethefocusofsuchanintensiveresearcheffort-andprovidinganamazingresourceforunderstandingthis speciesandgenomeevolutionmoregenerally.Finally,wehighlightthecontributionmadebythelateRichardZannwithhis studies of the ecology, physiology and behaviour of the wild Zebra Finch and his tremendous enthusiasm for the species. Richard would have welcomed the status that the Zebra Finch currently enjoys in science, and looked forward to the many exciting research opportunities that this supermodel species will continue to provide in the future. 'The Zebra Finch is a small Australian Ploceid which is ideally suitable for laboratory observations. It will nest and rear young in small indoor aviaries. New birds, transported to the laboratory in small boxes, will begin to nest-build and court within minutes of their release into an aviary. There are no seasonal difficulties, as it breeds all through the year. The species is exclusively a seed-eater and the nestlings require no special diet in captivity. The birds are not disturbed by the presence of an unconcealed human observer.' Desmond Morris (1954; Behaviour 6, 271-322).
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.
In many species that form socially monogamous pair bonds, a considerable proportion of the offspring is sired by extrapair males. This observation has remained a puzzle for evolutionary biologists: although mating outside the pair bond can obviously increase the offspring production of males, the benefits of such behavior to females are less clear, yet females are known to actively solicit extrapair copulations. For more than two decades adaptionist explanations have dominated the discussions, yet remain controversial, and genetic constraint arguments have been dismissed without much consideration. An intriguing but still untested hypothesis states that extrapair mating behavior by females may be affected by the same genetic variants (alleles) as extrapair mating behavior by males, such that the female behavior could evolve through indirect selection on the male behavior. Here we show that in the socially monogamous zebra finch, individual differences in extrapair mating behavior have a hereditary component. Intriguingly, this genetic basis is shared between the sexes, as shown by a strong genetic correlation between male and female measurements of extrapair mating behavior. Hence, positive selection on males to sire extrapair young will lead to increased extrapair mating by females as a correlated evolutionary response. This behavior leads to a fundamentally different view of female extrapair mating: it may exist even if females obtain no net benefit from it, simply because the corresponding alleles were positively selected in the male ancestors.
Zebra finch (Taeniopygia guttata) bills are sexually dichromatic with males possessing redder bills than females. Males with redder bills have been shown to be preferred as mates by females and to produce more offspring in laboratory experiments. In contrast, females with redder bills have suffered higher mortality and produced fewer offspring. In this paper, I report on a quantitative genetic study of male and female bill colour from a cross-fostering experiment. The heritability estimates for bill colour between parents and their biological offspring ranged from 0.23 to 0.58 and all but one of these estimates is significantly greater than zero. The heritability estimates between cross-fostered offspring and their non-biological parents were not significantly different from zero. Likewise, the genetic correlation between male and female bill colour was large (rg = 0.81) for parents and their biological offspring, but not for cross-fostered offspring and their non-biological parents. I also demonstrate the extent that the genetic correlation between the sexes can retard the predicted evolution of bill colour and create a selection load that reduces the expected reproduction of this laboratory population.
We examined natural and sexual selection in a laboratory population of zebra finches (Taeniopygia guttata), with a principal focus on bill color. Previous studies indicated that females prefer males with redder bills, whereas males prefer females with less red bills, For male red bill color, both the selection differential and selection gradient coefficients were significantly positive with fitness (the number of offspring surviving to independence), which was primarily due to differences in the time to the first nest and in reproductive rate but not to differences in survival. In contrast, for female red bill color, there was significant negative selection, which was due to differences in most stages of reproductive and survival selection but not to differences in the time to the first nest. There were no significant correlations between male or female bill color and offspring weight or postfledging survival. All male plumage color traits (breast band, cheek patch, flank patch) showed nonsignificant selection for increase in size due to both the time to the first nest and for reproductive rate but showed selection for decrease in size due to survival. Tarsus length was the only male trait to show significant selection for decrease in size, The opposing selection on red bill color between the sexes indicates that the positive genetic correlation between male and female red bill color may constrain the evolutionary rate of red bill sexual dichromatism.
One way that sexual selection for genetic benefits could operate in
monogamous species is through female choice during extra-pair
copulations (EPCS). EPCS are common in monogamous species, and field
studies are consistent with the hypothesis of females choosing
genetically attractive males for EPCS. Here I show that female zebra
finches actively solicit and perform EPCS with males that are more
attractive than their mates. Attractive males have higher song rates,
have sons with higher song rates, and fledge heavier offspring. This
provides a mechanism for sexual selection in monogamous species, and is
consistent with `good genes' models of sexual selection.
Bill color varies with age and sex in zebra finches. Among birds of similar age and condition, males' bills tend to be redder and darker than those of females, but there is overlap in the phenotypic expression of the sexes. The bills of young birds are paler and less red than those of older birds. There is also interindividual variation within age and sex class.
Experiments were performed to measure heterosexual and isosexual (= same sex) preferences of finches. Females preferred to associate with males with the reddest, brightest bills; they even preferred males whose bills were exaggerated through color applications of non‐toxic marking pen. Males preferred to associate with females with bill colors in the middle of the phenotypic range. Females thus have “directional” preferences for male bill color, whereas male preference is “stabilizing” with regard to female bill color.
In isosexual tests, neither sex showed a consistent preference for particular bill colors. Both sexes, however, displayed a tendency toward individual variability in preference. Bill color appears to be more important in heterosexual than in isosexual interactions.
Several authors have recently suggested that organisms prefer brightly colored mates because bright coloration indicates superior physical condition. Results reported here do not support this hypothesis. Alternative functional explanations for the observed preferences are that bill color signals mating status, age or reproductive value. None of these appears to be a cogent explanation for the trends. Preferences do not appear to result from sexual imprinting. The possibility that the preferences are aesthetic and non‐functional is discussed.
Recent years have seen a rapid expansion in the scope of quantitative genetic analyses undertaken in wild populations. We illustrate here the potential for such studies to address fundamental evolutionary questions about the maintenance of genetic diversity and to reveal hidden genetic conflicts or constraints not apparent at the phenotypic level. Trade-offs between differ-ent components of fitness, sexually-antagonistic genetic effects, maternal ef-fects, genotype-by-environment interactions, genotype-by-age interactions, and variation between different regions of the genome in localized genetic correlations may all prevent the erosion of genetic variance. We consider ways in which complex interactions between ecological conditions and the expression of genetic variation can be elucidated, and emphasize the ben-efits of conducting selection analyses within a quantitative genetic frame-work. We also review potential developments associated with rapid advances in genomic technology, in particular the increased availability of extensive marker information. Our conclusions highlight the complexity of processes contributing to the maintenance of genetic diversity in wild populations, and underline the value of a quantitative genetic approach in parameterizing models of life-history evolution.
The frequency of extra-pair parentage in a wild population of zebra finches Taeniopygia guttata was examined by DNA fingerprinting. A total of 25 families, comprising 16 pairs of parents and 92 offspring (in broods of 1 to 6) were examined. Ten cases of extra-pair parentage, presumed to constitute intraspecific brood parasitism, were detected (10.9% of offspring or 36% of broods), including one possible instance of quasi-parasitism (parasitism by a female fertilized by the male nest owner). The average number of parasitic eggs per clutch detected by fingerprinting was 1.100.32 SD, very similar to the one egg difference in average clutch size between parasitised (6.00.82) and unparasitised nests (5.00.95). Two cases of extra-pair paternity (EPP) were detected among 82 offspring whose maternity was confirmed: 2.4% of offspring, or 8% of broods. In both cases EPP accounted for only a single offspring within a brood. Behavioural observations show that EPP occurs through extra-pair copulation rather than rapid mate switching. The results are discussed in the light of what is known about the fertile period and sperm precedence patterns in this species.
Developmental stress has recently been shown to have adverse effects upon adult male song structure in birds, which may well act as an honest signal of male quality to discriminating females. However, it still remains to be shown if females can discriminate between the songs of stressed and non-stressed males. Here we use a novel experimental design using an active choice paradigm to investigate preferences in captive female zebra finches (Taeniopygia guttata). Nine females were exposed to ten pairs of songs by previously stressed and non-stressed birds that had learned their song from the same tutor. Song pairs differed significantly in terms of song complexity, with songs of stressed males exhibiting lower numbers of syllables and fewer different syllables in a phrase. Song rate and peak frequency did not differ between stressed and non-stressed males. Females showed a significant preference for non-stressed songs in terms of directed perching activity and time spent on perches. Our results therefore indicate that developmental stress affects not only the structure of male song, but that such structural differences are biologically relevant to female mate choice decisions.
Studies of female mate preference in zebra finches (Taenopygia guttata) have shown that male beak colour and song rate are important. However, the two characters are correlated. Here the effect of beak colour and song rate on female choice are examined independently. In mate choice tests involving two males, beak colour was manipulated artificially using nail varnish. The results showed that females showed a significant preference for males with a high song rate, but not with a red beak. Females did not prefer males with a red beak if song rate was low and females preferred males with orange beaks who expressed a high song rate. Female preference for males with red beaks was not found when beak and song characters were no longer correlated.
Good estimates of the genetic parameters of natural populations, such as heritability, are essential for both understanding
how genetic variation is maintained and estimating a population’s evolutionary potential. Long-term studies on birds are especially
amenable for calculating such estimates because of the ease with which pedigrees can be inferred. Recent ‘animal model’ methodology,
originally developed by animal breeders to identify animals of high genetic merit, has been applied to natural bird populations
of known pedigree. Animal models are more powerful than traditional analyses such as parent–offspring regression because they
use all of the available pedigree information simultaneously. In doing so, they can accommodate common phenomena like selection
and inbreeding and are especially suitable for the complex and incomplete pedigrees typical of natural populations. Animal
models not only provide a better way of estimating genetic and environmental variance components, they also allow individual
phenotypes to be separated into their genetic and environmental components. Here we aim to provide the interested ornithologist
with an accessible entry into the vast and sometimes daunting quantitative genetics literature and, in particular, into the
literature on the animal model. We outline not only the possibilities offered by the animal model for the accurate estimation
of genetic parameters in the wild but also associated potential pitfalls and limitations. On the whole, we aim to provide
an accessible and up-to-date overview of the rapidly developing and exciting field of evolutionary genetics applied to long-term
studies of wild bird populations.
The Zebra Finch (Taeniopygia guttata) is the first species of passerine bird with a complete genome sequence, making it an exciting time for avian evolutionary biology. Native to Australia and the Lesser Sunda Islands, this species has long played an important role in the study of ecology, behaviour and neuroscience. With the sequencing of its genome, the Zebra Finch now also represents an important model system for evolutionary and population genomics. The production of a genome sequence for the Zebra Finch will have far-reaching impacts on the study of avian biology. Here we discuss the genomic resources available for the Zebra Finch, including the genome sequence itself, and some of the ways in which they will facilitate the study of avian diversity. We also highlight recent examples from the literature that have already begun to leverage Zebra Finch genomic tools towards the study of birds in nature.
Many traits are genetically correlated with each other. Thus, selection that changes the mean value of one trait causes other traits to change as well. Recent comparative studies have emphasized the possible importance of such correlated responses in affecting the evolution of traits, including some behaviors, which are of little adaptive significance, or even maladaptive. However, it is also possible for traits with major effects on fitness, such as brain size, to evolve entirely by correlated response. Other traits that do not appear to have evolved at all may have been subject to much directional selection, simply to prevent their evolution by correlated response. The new interest in correlated responses reflects more rigorous attempts to consider the organism as a whole, rather than dissecting it into a number of questionably separable traits.
Differential reproductive investment by the mother can critically influence offspring development and phenotype, and strong selection is therefore expected to act on such maternal effects. Although a genetic basis is a prerequisite for phenotypic traits to respond to selection and thus to evolve, we still know very little about the extent of heritable variation in maternal effects in natural populations. Here, we present the first estimates of intrafemale repeatability across breeding seasons and estimates of heritability of hormone-mediated maternal effects in a wild population of collared flycatchers (Ficedula albicollis). We found that maternal yolk testosterone (T) concentrations, yolk mass, and egg mass were moderately to highly repeatable within females across years, whereas intrafemale consistency of maternal yolk androstenedione (A4) deposition was low yet statistically significant. Furthermore, maternal yolk T transfer, yolk mass, and egg mass were significantly heritable, whereas yolk A4 transfer was not. These results strongly suggest that two major maternal yolk androgens are differentially regulated by genes and the environment. Selection on heritable variation in maternal yolk T deposition has the potential to shape the rate and direction of phenotypic change in offspring traits and can thereby accelerate or impede the response to selection in natural populations.
We estimated the heritability and genetic correlation between male and female bill colour in a laboratory population of zebra finches (Taeniopygia guttata) in order to examine the potential genetic constraints on the evolution of a sexually dimorphic trait. The heritability estimates of bill colour from regressions of offspring on single parents ranged from h2 = 0.34 to 0.73 and all but one of these estimates were significantly greater than zero. The restricted maximum likelihood heritability estimates for full- and half-siblings were significant for females (h2 = 0.48) but not significant for males (h2 = 0.45). The maximum likelihood estimates indicate that there is little dominance genetic variance for bill colour. The large genetic correlation between male and female bill colour (rg = 0.91) combined with opposing selection on male and female bill colour indicates that the evolution to sex-specific optima may proceed very slowly.
Good-genes hypotheses of sexual selection predict that offspring fathered by preferred males should have increased viability
resulting from superior genetic quality. Several studies of birds have reported findings consistent with this prediction,
but maternal effects are an important confounding variable. Those studies that have attempted to control for maternal effects
have only considered differential maternal investment after egg laying. However, female birds differentially deposit testosterone
in the eggs, and this influences the development of the chick. This study shows that female birds deposit higher amounts of
testosterone and 5α-dihydrotestosterone in their eggs when mated to more attractive males.
This book focuses on drosophila as an especially useful model organism for exploring questions of evolutionary biology in the full range of evolutionary studies: population genetics, ecology, ecological genetics, speciation, phylogenetics, genome evolution, molecular evolution, and development. The author presents an integrated view of evolutionary biology as elucidated in this single organism. Special effort is made to point out holes in our knowledge and areas particularly ripe for new investigation.
Mothers have the ability to profoundly affect the quality of their offspring from the size and quality of their eggs to where, when, and how eggs and young are placed, and from providing for and protecting developing young to choosing a mate. In many instances, these maternal effects may be the single most important contributor to variation in offspring fitness. This book explores the wide variety of maternal effects that have evolved in plants and animals as mechanisms of adaptation to temporally and spatially heterogeneous environments. Topics range from the evolutionary implications of maternal effects to the assessment and measurement of maternal effects. Four detailed case studies are also included. This book represents the first synthesis of the current state of knowledge concerning the evolution of maternal effects and their adaptive significance.
Studies of female mate preference in zebra finches (Taenopygia guttata) have shown that male beak colour and song rate are important. However, the two characters are correlated. Here the effect of beak colour and song rate on female choice are examined independently. In mate choice tests involving two males, beak colour was manipulated artificially using nail varnish. The results showed that females showed a significant preference for males with a high song rate, but not with a red beak. Females did not prefer males with a red beak if song rate was low and females preferred males with orange beaks who expressed a high song rate. Female preference for males with red beaks was not found when beak and song characters were no longer correlated.
For some species in which family members are dependent on or are in close proximity to one another, a character may be composed of several conceptual components, some being contributed by related individuals. A general expression for the genotypic covariance between relatives is synthesized for such characters when mating is random. The relationships between individuals contributing to a measure of the character are important in defining the genotypic variance and the response to selection. A character of an offspring influenced by a maternal effect illustrates the expression.
Two way choice tests show a preference of female zebra finches for male songs four standard deviations longer than normal song. Further tests show the ontogeny of this preference to parallel song learning in general as well as a preference for songs with entirely heterogeneous notes compared to songs with four note repeats. These findings are discussed in relation to a theory of the evolution of bird song from bird calls due to female preferences for longer, more complex vocalizations.
Birds are a particularly good group with which to examine the importance of maternal effects, as parental contributions can be relatively easily quantified compared with other groups. There have undoubtedly been more studies on maternal effects in the Zebra Finch than any other single bird species. Studies of this species have examined the importance of maternal effects mediated through sex allocation, size, nutrients and hormones of of eggs, incubation behaviour and provisioning levels. A synthesis of all of this work illustrates some contrasting results (e.g. many high-profile results have failed to be replicated), some very common patterns (e.g. investment shifts through the laying sequence), and potentially interesting and complex interactions between traits (e.g. between sex of offspring and hormonal profiles of eggs). This extensive collection of work on the Zebra Finch provides useful general insight into the patterns of maternal investment in birds and the effects on offspring phenotype. However, we caution that the literature is probably littered with studies that have overemphasised the importance of some maternal effects and recent studies have highlighted analytical and logical flaws that have probably led to misplaced confidence in some of the findings reported to date. Finally, it is worth considering that the bulk of the literature is based on studies of captive domesticated birds and ecological and physiological data from individuals in the wild is currently lacking. The biological relevance of maternal effects documented in this model species is therefore unclear.
The Zebra Finch Taeniopygia guttata is a model passerine and since the mid-1980s my research group has studied both domesticated birds in captivity, and wild birds in Australia, as part of a program of research designed to explore the adaptive significance and underlying mechanisms of sperm competition in birds. Extra-pair courtship is common in wild Zebra Finches, but rarely leads to mounting and as a result extra-pair paternity is infrequent, a result consistent with male Zebra Finch reproductive anatomy. Nonetheless, the species has proved to be an excellent model for sperm competition studies because its basic reproductive anatomy and reproductive processes are similar to other birds. The outcome of sperm competition in the Zebra Finch and other birds is best predicted by the passive sperm loss model, allowing for differences in sperm numbers and quality (fertilising capacity). Last male sperm precedence is not a 'rule' in birds but is a consequence of the way sperm competition experiments have been conducted. Several male reproductive traits, including sperm size and velocity in the Zebra Finch have a genetic basis, and, as the Zebra Finch genome project gains momentum, the genes for these traits will be identified.
During the last decades more and more attention has been focused on the function of the stress hormone corticosterone in free-living birds. Normally birds have low circulating levels of corticosterone throughout the year, but when exposed to a stressor they will, however, rapidly increase the corticosterone secretion, and thereby adjust their phyiology and behaviour to the new situation. To avoid chronic effects of high corticosterone levels the secretion rate returns to basal as soon as the alternate behaviour has been established or when the individual in some other way has succeeded to cope with the stressor. In short, elevated corticosterone levels will redirect behaviour away from reproduction towards survival, for example by stimulating dispersal and/or foraging behaviour. However, a bird must be able to modulate the adrenocortical stress response as one and the same response will have different biological effects in different ecological situations. So that at a certain time the bird should react rapidly to a stressor, whereas in another situation it should have a suppressed response to the same stressor. Thus, it is the adrenocortical stress response at a particular time, and not the basal corticosterone level, that affects an individuals' fitness and consequently the target for evolutionary forces. This paper reviews studies dealing with the adrenocortical stress response in birds. A major hypothesis is that seasonal modulations of an acute stress response should be found basically in species with short breeding seasons and/or in species breeding in severe environments. Although the patterns differ between species, most studies support this hypothesis. As a stress induced elevation of corticosterone levels can disrupt reproductive functions and reduce reproductive succees birds not only modulate their adrenocortical stress response on a seasonal basis, but also within or between populations. Among populations in, a species breeding in a wide variety of habitats those breeding in a more unpredictable and severe habitat normally are less sensitive to environmental Stressors. Consequently individuals in such a population have a suppressed adrenocortical stress response to an acute stressor. There are, however, some interesting exceptions to this rule. The selective forces behind these differences are so far unknown. In addition there are normally large inter-individual variations, as well as sex related differences, in the adrenocortical stress response. It has been suggested that individuals with large fat depots should be the ones to be more resistent to acute stress as they are less likely to be affected by, for example, severe weather conditions. Furthermore, it has been hypothesised that the sex investing most in parental responsibilities should reduce the adrenocortical stress response to avoid in duction of a corticosterone mediated escape behaviour. Results from different studies are however not always consistent with these hypotheses, and the bases for individual variations are today unclear. The adrenocortical stress response is also discussed in relation to social hierarchies and migratory strategies.
This chapter discusses the physiology, ecology, and behavior of hormones in avian eggs. The main source of hormones found in avian eggs is the maturing follicles of the female ovary that contain specialized cells creating different hormones during their development. The granulosa cells of the largest preovulatory follicles (F1) are the main source of circulating progesterone. Theca cells produce both estrogen and androgens, and the production decreases with increasing follicular maturation. Postovulatory follicles continue to produce steroids before final atresia, and their low androgen production during incubation is brought about by a decrease in luteinizing hormone stimulation rather than by a reduction of the steroidogenic capacity of the theca interna cells at that stage. Although sexual differentiation takes place in the early embryo by the means of processes based on estradiol, the development of sexually selected characters in birds is tightly linked to hormonal processes in adulthood, of both androgenic and estrogenic nature. While within‐brood distributions of yolk androgens can be highly species‐specific, many differential patterns can be found within the same species. Given the effects of androgens in chick competitiveness, females could use within‐clutch distributions of androgens to balance or reinforce the effects of hatching asynchrony.
Most of the characteristics studied by avian ecologists relate to the external appearance of birds¡ªmorphology, life history, behavior, and in some cases, physiology: the very characteristics upon which natural selection operates. These traits are likely to be the products of tens or hundreds of loci, and their expression can be modified by numerous environmental factors (Lynch and Walsh, 1998; Falconer and Mackay, 1996). The study of the emergent and evolutionary properties of this type of multifactorial inheritance is known as quantitative genetics, and it is based on indirect statistical inference rather than direct observation of specific loci and their gene products. The theory of quantitative genetics has been subject to considerable empirical scrutiny, and its successful application in plant and animal breeding testifies to its practical utility (Lynch and Walsh, 1998; Falconer and Mackay, 1996; Hill and Mackay, 1991; Mather and Jinks, 1982)
and Summary
The distance call (DC) of the offspring of wild‐caught zebra finches (ZF) was studied. Half the clutch (FR) was cross‐fostered to Bengalese finches (BF) until 40 or 60 days after hatching whereupon they were reunited with their normal reared sibs (NR) and caged in a separate room which held other similarly treated ZF. At day 100 the DC was recorded.
1. Female DCs of NR and FR groups were only slightly different and were very similar to the mothers' DC.
2. All FR males gave DCs that were completely different from their NR siblings and genetic fathers.
3. Some 16% of FR males learnt the DC of the BF fosters: the call of either the mother or the father.
4. Some 60% of FR males gave a typically ZF male call except that the noise element, the most sexually diagnostic feature of the DC, was entirely absent. There were no differences in the frequency of maximum amplitude (FMA), fundamental frequency (FF) or total duration of the call (TDC).
5. Some 30% of NR sons gave DCs identical to that of their father and the remainder showed strong resemblances so that the between family variation for sons was significantly greater than within family variation for three of four parameters; daughters were only significant for one parameter.
6. The duration of parental contact for 40 or 60 days had no significant effect on the outcome of the experiment.
7. Captivity did not affect the development of the DC.
Zusammenfassung
Der Distanzruf (Lockruf) (DC) des australischen Zebrafinken (ZF) wurde an Wildfangnachkommen untersucht. Hierzu wurde jeweils die Hälfte eines Geleges (FR) Japanischen Mövchen (BF) zur Aufzucht unterlegt. Im Alter von 40 bzw. 60 Tagen wurden diese Jungtiere von den Stiefeltern getrennt und mit ihren von den eigenen Eltern aufgezogenen Geschwistern (NR) zusammengesetzt. Sie wurden in einem Raum untergebracht, in dem sich ausschließlich Zebrafinken mit ähnlicher Vorgeschichte befanden. Im Alter von 100 Tagen wurden die Distanzrufe auf Tonband aufgenommen.
1. Die Distanzrufe der NR‐Weibchen unterschieden sich nur geringfügig von denen der FR‐Weibchen. Der jeweils entwickelte Distanzruf ähnelte sehr dem der natürlichen Mutter.
2. Die Distanzrufe aller FR‐Männchen unterschieden sich dagegen sehr deutlich sowohl von denen ihrer Geschwister aus der Gruppe NR als audi von denen ihrer leiblichen Väter.
3. Etwa 16% der FR‐Männchen lernten den Distanzruf der Stiefeltern, und zwar entweder den der Mutter oder den des Vaters.
4. Etwa 60% der FR‐Männchen entwickelten einen zebrafinken‐typischen männlichen Distanzruf, dem jedoch der geräuschhafte Teil des Rufes (noise element) fehlte, der normalerweise das ausgeprägteste Unterscheidungsmerkmal des männlichen Rufes darstellt. Keine Unterschiede bestanden dagegen bezüglich der Frequenz der maximalen Amplitude (FMA), der Grundfrequenz (FF) oder der Gesamtdauer des Rufes (TDC).
5. Etwa 30% der NR‐Männchen entwickelten einen Distanzruf, der mit dem des Vaters übereinstimmte; bei den übrigen Tieren war ebenfalls eine deutliche Ähnlichkeit festzustellen. Somit erwies sich für drei von vier gemessenen Parametern die Variation zwischen Familien als signifikant höher als die Variation innerhalb einer Familie. Bei Weibchen war dieser Unterschied nur für einen Parameter nachzuweisen.
6. Die Dauer des Kontaktes mit den Eltern bzw. Stiefeltern (40 bzw. 60 Tage) hatte keinen signifikanten Einfluß auf die Rufentwicklung.
7. Gefangenschaftsbedingungen haben keinen Einfluß auf die Entwicklung des Distanzrufes.
8. Der Distanzruf entwickelt sich aus den Bettelrufen, und seine Vorstufe (LTC) tritt erstmals vor dem 15. Lebenstag auf. Der Distanzruf verändert sich mit zunehmendem Alter und erreicht seine endgültige Form bei den Weibchen mit etwa 40, bei den Männchen mit 60–80 Tagen. Vor dem 35. bis 40. Lebenstag sind keine geschlechtsspezifischen Unterschiede festzustellen. Im darauffolgenden Zeitraum von 10 bis 20 Tagen erfolgt dagegen bei den Männchen eine ausgeprägte Veränderung des Frequenz‐verlaufes im zweiten Teil des Rufes. Bei den NR‐Männchen entsteht durch diesen Prozeß der geräuschhafte Anteil des Rufes. Bei den meisten FR‐Männchen fehlt dieser stark modulierte Anteil.
Die Ergebnisse lassen den Schluß zu, daß der Distanzruf den Zebrafinken‐Männchen nicht angeboren ist und daß vor allem der geräuschhafte Anteil des Distanzrufes des Vaters gehört werden muß. Einige Charakteristika des Rufes scheinen allerdings genetisch fixiert zu sein, doch kann dieses Grundmuster unter bestimmten Umständen (Fremdaufzucht) durch die angeborene Tendenz junger Männchen, den Ruf des Vaters (hier: Stiefvaters) zu erlernen, überdeckt werden. Für die Entwicklung des Distanzrufes junger Weibchen spielen solche Umwelteinflüsse dagegen nahezu keine Rolle. Die biologische Bcdeutung dieser Unterschiede wird diskutiert, und Gesang und Distanzruf werden im Hinblick auf ihre ontogenetische und phylogenetische Entwicklung miteinander verglichen.
1. Females of egg‐laying vertebrates may adjust the development of their offspring to prevailing environmental conditions by regulating the deposition of hormones into their eggs. Within‐ and amng‐clutch variation in levels of steroid hormones were studied in the egg yolks of the Black‐Headed Gull ( Larus ridibundus , Linnaeus) in relation to environmental conditions at the nest site. This species breeds in colonies of different densities and in different habitats, and the chicks hatch asynchronously.
2. Egg yolks contained very high levels of androstenedione, substantial levels of testosterone and moderate levels of 5α‐dihydrotestosterone. Oestrogen (17β‐oestradiol) was not detected.
3. Androgen levels increased strongly with laying order, irrespective of egg or yolk mass. This may compensate for the disadvantages of the later hatching chicks. These results have implications for adaptive hypotheses that were proposed for asynchronous incubation.
4. Eggs of lighter clutches contained more androgens, perhaps to compensate for a lower nutritional quality of these eggs.
5. Birds breeding in the periphery of a colony, being relatively more aggressive and having relatively large territories, laid eggs that contained more androgens than those of birds breeding in the centre. These high yolk androgen levels may facilitate growth and motor development of the chicks, which may be especially important for chicks developing at the periphery of a colony. Reduced levels may be adaptive for birds breeding in the centre, where risk of infectious diseases is high, since steroids may be immunosuppressive.
6. Corrected for nest distance, clutches of birds in high vegetation, where predation risk is less severe and therefore competition for nest sites perhaps high, contained relatively high levels of androgens. It is suggested that the level of yolk androgens reflects the hormonal condition of the female, that in turn is influenced by her characteristics such as her age and aggressiveness, and the level of social stimulation.
High breeding density can cause elevated plasma androgen levels in adult birds. Since maternal androgens are deposited into egg yolk, high breeding density may result in elevated yolk androgen levels as well.
The relationship between breeding density and yolk androgen levels was examined in the European Starling, Sturnus vulgaris . The concentration and total content of yolk androstenedione and yolk testosterone were measured in eggs from 24 clutches distributed across nine different colonies of nestboxes.
Yolk androstenedione and testosterone levels were significantly higher in colonies where a greater proportion of nestboxes had active nests.
Yolk testosterone levels were significantly higher, and yolk androstenedione levels were marginally higher, in colonies with a greater absolute number of active nests.
Yolk androgen levels were not related to the number of active nests in adjacent nestboxes.
We conclude that female starlings nesting in colonies with higher breeding densities transfer more androgen to their eggs.
This relationship may be mediated by increased interfemale aggression, particularly towards floater females searching for mates or nests to brood parasitize, in high‐density colonies. Such a relationship between maternal environment and maternal yolk androgens may represent adaptive maternal modification of offspring phenotype or a non‐adaptive physiological constraint which females cannot avoid.
Summary 1. Classical evolutionary theory states that senescence should arise as a consequence of the declining force of selection late in life. Although the quantitative genetic predictions of hypotheses derived from this theory have been extensively tested in laboratory studies of invertebrate systems, relatively little is known about the genetics of ageing in the wild. 2. Data from long-term ecological studies is increasingly allowing quantitative genetic approaches to be used in studies of senescence in free-living populations of vertebrates. We review work to date and argue that the patterns are broadly consistent with theoretical predictions, although there is also a clear need for more empirical work. 3. We argue that further advances in this field of research might be facilitated by increased use of reaction norm models, and a decreased emphasis on attempting to discriminate between mutation accumulation and antagonistic pleiotropy models of senescence. We also suggest a framework for the better integration of environmental and genetic effects on ageing. 4. Finally, we discuss some of the difficulties in applying quantitative genetic models to studies of senescence outside the laboratory. In particular we highlight the problems that viability selection can cause for an accurate estimation of parameters used in the prediction of age-trajectory evolution.
To study the population genetics as well as the mating system of captive zebra finch (Taeniopygia guttata) populations, we developed primers for 12 microsatellite loci and screened them in 529 individuals from two successive generations of a single captive population. All markers were polymorphic with five to 14 alleles per locus. We checked all markers for Mendelian inheritance in 307 offspring whose parents were known for sure. Four markers showed evidence for the presence of null alleles. Once allowing for null alleles, we found no mismatches between offspring and parents, suggesting a very low rate of mutation. Average observed and expected heterozygosities across the eight loci showing no evidence for null-alleles was 0.819 and 0.812, respectively.
— The ability of populations to undergo adaptive evolution depends on the presence of quantitative genetic variation for ecologically important traits. Although molecular measures are widely used as surrogates for quantitative genetic variation, there is controversy about the strength of the relationship between the two. To resolve this issue, we carried out a meta-analysis based on 71 datasets. The mean correlation between molecular and quantitative measures of genetic variation was weak (r = 0.217). Furthermore, there was no significant relationship between the two measures for life-history traits (r =−0.11) or for the quantitative measure generally considered as the best indicator of adaptive potential, heritability (r =−0.08). Consequently, molecular measures of genetic diversity have only a very limited ability to predict quantitative genetic variability. When information about a population's short-term evolutionary potential or estimates of local adaptation and population divergence are required, quantitative genetic variation should be measured directly.
To estimate the metabolic costs of regrowth of reproductive organs and formation of eggs, we compared the resting metabolic rate (RMR) of female great tits (Parus major) during the periods of ovarian recrudescence, egg laying, nestling feeding and during winter. We found RMR of individual females, as measured in an open circuit respirometer during night, to be significantly higher during all the breeding phases when compared to measurements during the winter. Females had a 12% increase in RMR during the nest-building phase, an increase of 27% during egg production and an increase of 20% during the chick feeding phase compared to RMR during winter. However, we found no significant difference in energy expenditure during the night between females producing eggs and females feeding chicks. A causal link between RMR and egg production was further confirmed by females producing large eggs having a higher RMR than females producing small eggs. Mass-specific RMR increased steadily from the winter throughout the breeding season, being highest when females were feeding their nestlings. Thus, even though females did not produce ovary-oviduct tissue or eggs during chick feeding, they had a very high RMR. We conclude that the biosynthetic cost of egg formation will probably not limit clutch size but may well, together with the cost of ovary-oviduct recrudescence, influence the timing of reproduction. We suggest that the high RMR of females feeding nestlings, probably is due to an increase in size and efficiency of the alimentary tract, needed to sustain a high rate of energy turnover during this period.
Male Zebra Finches (Taeniopygia guttata) sing a unique, stereotyped song that they learn from a tutor during development. A set of interconnected areas of the brain work together so that the birds can perceive, learn and produce song. In this review, we introduce the major components of the song system and describe evidence for how each might contribute to these three aspects of song. In particular, we highlight studies that have measured patterns of gene expression in the song system. These experiments clarify the structural organisation, and reveal functional activities, of the neural system underlying vocal communication. The utility of gene expression studies has been greatly enhanced with the release of the Zebra Finch genome. Investigation of gene expression in the song system will therefore continue to be a powerful way to connect the workings of this neural circuit with the behaviour of song.
Androgenic hormones occur naturally in bird egg yolk and are known to enhance growth in canary and gull chicks. Gil et al. (1999, Science, 286, 126–128) have recently proposed that female allocation of androgens to eggs represents a form of costly maternal investment. This hypothesis predicts that females of high quality or high reproductive potential should invest more yolk androgens in their eggs than females of low quality or low reproductive potential. We tested these predictions by examining interfemale variation in allocation of the androgenic steroids testosterone and androstenedione to eggs in a wild population of European starlings, Sturnus vulgaris. We collected 30 full clutches of eggs and captured 22 of the females that laid these clutches for phenotypic measurements. In agreement with the hypothesis, we found that there was significant interfemale variation in yolk androgen concentrations. Furthermore, older females deposited more androstenedione and testosterone in eggs than 1-year-old females, and females laying early or large clutches deposited more testosterone in eggs than females laying late or small clutches. However, females in good body condition did not deposit more androgens in eggs than females in poor body condition. Large-yolked eggs had a higher total yolk androgen content than small-yolked eggs, but larger eggs did not have higher concentrations of yolk androgens. The results in general support the investment hypothesis of yolk androgen allocation. However, further data are needed regarding the costs of yolk androgen allocation and the effects of yolk androgens on offspring to substantiate the assumptions of the hypothesis. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.
Numerous studies have measured the mating preferences of female zebra finches, Taeniopygia guttata, using choice-chamber experiments, but no study has focused on how consistent individual females are in their choices and the extent to which females agree on their preferences, although these questions are of great conceptual importance. We conducted a large number of mate choice trials involving unmanipulated stimulus males, and found low but significant consistency (repeatability of time allocation by a female tested twice with the same set of males R = 0.29), and very low but significant between-female agreement (different females tested with the same set of males: R = 0.11). Although low individual consistency indicates that preferences were relatively weak or hard to measure, we found significant repeatability of individual preference functions with regard to beak colour, song rate and male aggressiveness when individual females were tested twice with different sets of males. This means that some females consistently preferred red-beaked males whereas others preferred orange-beaked males, some preferred high and others low song rates, and some preferred aggressive and others less aggressive males. Of these male traits, only song rate was positively related to average male attractiveness. Low between-female agreement did not seem to result from assortative mating for quality, because there was no repeatability of an individual female's preference for attractive or unattractive males. It is possible that disagreement follows from choice for genetic compatibility, but much of it could also result from weak preferences and little variation in male quality.
To advance our understanding of biological processes we often plan our experiments based on published data. This can be confusing though, as data from experiments performed in a laboratory environment are sometimes different from, or completely opposite to, findings from similar experiments performed in the “real world”. In this mini-review, we discuss instances where results from laboratory experiments differ as a result of laboratory housing conditions, and where they differ from results gathered in the field environment. Experiments involving endocrinology and behavior appear to be particularly susceptible to influence from the environment in which they are performed.As such, we have attempted to promote discussion of the influence of housing environment on the reproductive axis, circadian biology and behavior, immune function, stress biology, neuroplasticity and photoperiodism. For example, why should a rodent species be diurnal in one housing environment yet nocturnal in another? Are data that are gathered from experiments in the laboratory applicable to the field environment, and vice-versa? We hope not only to highlight the need for experiments in both lab and field when looking at complex biological systems, but also to promote frank discussion of discordant data. Perhaps, just as study of individual variation has been gaining momentum in recent years, data from variation between experimental arenas can provide us with novel lines of research.
Zebra finches are an important model for vocal learning and avian mate choice. The two are contingent on each other: males' learned songs are addressed at females with learned preferences. This review documents the recent changes away from a purely mechanism-orientated approach of song learning toward the question of how variation in male phenotypic quality is reflected by variation in male song. The substantial evidence for female song preference learning is reviewed and compared to what is known to about unlearned preference biases. From the complementary evidence, a picture emerges that shows how cultural transmission of the male mating signal is paralleled by sensory learning processes on the receiver's side. The question of how the trait and preference might react in concert to environmental change and how learned receiver biases affect the evolutionary dynamics of culturally transmitted song emerge as exciting future research prospects.
An absence of genetic variance in traits under selection is perhaps the oldest explanation for a limit to evolutionary change, but has also been the most easily dismissed. We review a range of theoretical and empirical results covering single traits to more complex multivariate systems, and show that an absence of genetic variance may be more common than is currently appreciated. From a single-trait perspective, we highlight that it is becoming clear that some trait types do not display significant levels of genetic variation, and we raise the possibility that species with restricted ranges may differ qualitatively from more widespread species in levels of genetic variance in ecologically important traits. A common misconception in many life-history studies is that a lack of genetic variance in single traits, and genetic constraints as a consequence of bivariate genetic correlations, are different causes of selection limits. We detail how interpretations of bivariate patterns are unlikely to demonstrate genetic limits to selection in many cases. We advocate a multivariate definition of genetic constraints that emphasizes the presence (or otherwise) of genetic variance in the multivariate direction of selection. For multitrait systems, recent results using longer term studies of organisms, in which more is understood concerning what traits may be under selection, have indicated that selection may exhaust genetic variance, resulting in a limit to the selection response.
We report the first study with the aim to estimate heritability in a wild population, a nest box breeding population of blue tits. We estimated heritability as well as genetic and phenotypic correlations of resting metabolic rate (RMR), body mass and tarsus length with an animal model based on data from a split cross-fostering experiment with brood size manipulations. RMR and body mass, but not tarsus length, showed significant levels of explained variation but for different underlying reasons. In body mass, the contribution to the explained variation is mainly because of a strong brood effect, while in RMR it is mainly because of a high heritability. The additive variance in RMR was significant and the heritability was estimated to 0.59. The estimates of heritability of body mass (0.08) and tarsus length (0.00) were both low and based on nonsignificant additive variances. Thus, given the low heritability (and additive variances) in body mass and tarsus length the potential for direct selection on RMR independent of the two traits is high in this population. However, the strong phenotypic correlation between RMR and mass (0.643 +/- 0.079) was partly accounted for by a potentially strong, although highly uncertain, genetic correlation (1.178 +/- 0.456) between the two traits. This indicates that the additive variance of body mass, although low, might still somewhat constrain the independent evolvability of RMR.
There are several possible explanations for the female preference for male repertoires in birds. These males are older, and have better territories; thus there are functional reasons for females to prefer these males. However, there is an alternative explanation; females may habituate less quickly to song repertoires than single songs. I tested whether females have a non-functional, sensory bias for male song repertoires, by testing female preference for a repertoire in zebra finches (Taenopygia guttata), a species in which males possess a single stereotyped song. Females chose between a male repertoire of four different phrases created from the song phrase of one individual and that of one of those phrases repeated four times (natural zebra finch song). Females were also given a choice between the above repertoire and a song made from the phrases of four related males ('family' stimulus). I tested female preference by training females to press a button for presentation of a song stimulus, and counting the number of button presses. Females preferred the song repertoire to a single phrase song, and did not differentiate between the repertoire and song phrases from four males. Evidence from the Estrildidae indicates that having a single song is the ancestral state for zebra finches, so the preference is not ancestral.
Animal vocalizations play an important role in individual recognition, kin recognition, species recognition, and sexual selection. Despite much work in these fields done on birds virtually nothing is known about the heritability of vocal traits in birds. Here, we study a captive population of more than 800 zebra finches (Taeniopygia guttata) with regard to the quantitative genetics of call and song characteristics. We find very high heritabilities in nonlearned female call traits and considerably lower heritabilities in male call and song traits, which are learned from a tutor and hence show much greater environmental variance than innate vocalizations. In both sexes, we found significant heritabilities in several traits such as mean frequency and measures of timbre, which reflect morphological characteristics of the vocal tract. These traits also showed significant genetic correlations with body size, as well as positive genetic correlations between the sexes, supporting a scenario of honest signaling of body size through genetic pleiotropy ("index signal"). In contrast to such morphology-related voice characteristics, classical song features such as repertoire size or song length showed very low heritabilities. Hence, these traits that are often suspected to be sexually selected would hardly respond to current directional selection.
Divergent selection pressures among populations can result not only in significant differentiation in morphology, physiology and behaviour, but also in how these traits are related to each other, thereby driving the processes of local adaptation and speciation. In the Australian zebra finch, we investigated whether domesticated stock, bred in captivity over tens of generations, differ in their response to a life-history manipulation, compared to birds taken directly from the wild. In a 'common aviary' experiment, we thereto experimentally manipulated the environmental conditions experienced by nestlings early in life by means of a brood size manipulation, and subsequently assessed its short- and long-term consequences on growth, ornamentation, immune function and reproduction. As expected, we found that early environmental conditions had a marked effect on both short- and long-term morphological and life-history traits in all birds. However, although there were pronounced differences between wild and domesticated birds with respect to the absolute expression of many of these traits, which are indicative of the different selection pressures wild and domesticated birds were exposed to in the recent past, manipulated rearing conditions affected morphology and ornamentation of wild and domesticated finches in a very similar way. This suggests that despite significant differentiation between wild and domesticated birds, selection has not altered the relationships among traits. Thus, life-history strategies and investment trade-offs may be relatively stable and not easily altered by selection. This is a reassuring finding in the light of the widespread use of domesticated birds in studies of life-history evolution and sexual selection, and suggests that adaptive explanations may be legitimate when referring to captive bird studies.