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1.  No Band Color Effects on Male Courtship Rate or Body Mass in the Zebra Finch: Four Experiments and a Meta-Analysis 
PLoS ONE  2012;7(6):e37785.
Replication of experiments is essential for distinguishing real effects from type 1 errors and idiosyncrasies. One of the most replicated experiments in behavioral ecology is the presumed manipulation of male attractiveness in zebra finches by adding red or green color bands. Red-banded males were found to have higher fitness than green-banded males, and most empirical evidence suggests that this effect is mediated by female mating preferences rather than by male-male competition. A recent study, however, reported that color bands affected male courtship rate and body mass independently of female behavior. If this effect was real, some earlier findings of female preferences and maternal effects on offspring traits could potentially be reinterpreted as being mediated indirectly via effects on male behavior. This new perspective seems appealing also in light of a growing interest in bi-directional feedback mechanisms between endocrinology and ornamentation. However, here we report four independent failures to replicate this effect of color bands on courtship rate and body mass. Combining this new experimental data with all the published evidence in a meta-analysis shows that color bands seem to affect neither male courtship rate (average effect size d = 0.02) nor male body mass (d = −0.07). The present case is a reminder that replication of experiments lies at the heart of distinguishing between real effects and false positive findings.
doi:10.1371/journal.pone.0037785
PMCID: PMC3369886  PMID: 22685545
2.  Correlates of male fitness in captive zebra finches - a comparison of methods to disentangle genetic and environmental effects 
Backgound
It is a common observation in evolutionary studies that larger, more ornamented or earlier breeding individuals have higher fitness, but that body size, ornamentation or breeding time does not change despite of sometimes substantial heritability for these traits. A possible explanation for this is that these traits do not causally affect fitness, but rather happen to be indirectly correlated with fitness via unmeasured non-heritable aspects of condition (e.g. undernourished offspring grow small and have low fitness as adults due to poor health). Whether this explanation applies to a specific case can be examined by decomposing the covariance between trait and fitness into its genetic and environmental components using pedigree-based animal models. We here examine different methods of doing this for a captive zebra finch population where male fitness was measured in communal aviaries in relation to three phenotypic traits (tarsus length, beak colour and song rate).
Results
Our case study illustrates how methods that regress fitness over breeding values for phenotypic traits yield biased estimates as well as anti-conservative standard errors. Hence, it is necessary to estimate the genetic and environmental covariances between trait and fitness directly from a bivariate model. This method, however, is very demanding in terms of sample sizes. In our study parameter estimates of selection gradients for tarsus were consistent with the hypothesis of environmentally induced bias (βA = 0.035 ± 0.25 (SE), βE = 0.57 ± 0.28 (SE)), yet this differences between genetic and environmental selection gradients falls short of statistical significance.
Conclusions
To examine the generality of the idea that phenotypic selection gradients for certain traits (like size) are consistently upwardly biased by environmental covariance a meta-analysis across study systems will be needed.
doi:10.1186/1471-2148-11-327
PMCID: PMC3229482  PMID: 22067225
3.  A polymorphism in the oestrogen receptor gene explains covariance between digit ratio and mating behaviour 
In vertebrates, including humans, the relative length of the second to the fourth digit correlates with sex hormone-dependent behavioural, psychological and physiological traits. However, despite a decade of research, the underlying mechanism linking digit ratio to these sex hormone-dependent traits remains unclear. Previous work suggests that during embryo development, circulating levels of plasma androgens or oestrogens may act through their receptors to affect transcription levels of posterior HOX genes in the developing digits, thereby possibly influencing their relative length. The correlation between digit ratio and sex hormone-dependent traits might thus stem from variation in expression or sensitivity of the sex hormone receptors, or from variation in sex hormone levels in the embryo. Here, we show that in a population of 1156 zebra finches Taeniopygia guttata, a polymorphism in the oestrogen receptor α gene (ESR1) explains 11.3 per cent of the variation in digit ratio, and is also associated with male and female-mating behaviour. By contrast, we found no associations between digit ratio or mating behaviours and polymorphisms in the androgen receptor gene. Thus, our results (i) provide an explanation for the observed significant genetic covariance between digit ratio and male and female mating behaviour and (ii) strongly confirm the indicator function of digit ratio through the oestrogen pathway. Finally, we note that the commonly invoked effect of foetal testosterone on human digit ratio seems to be substantially weaker than the effect described here.
doi:10.1098/rspb.2010.1007
PMCID: PMC2981936  PMID: 20534613
2D : 4D; finger length; HOX genes; sexual behaviour; sex hormones
4.  Trisomy and triploidy are sources of embryo mortality in the zebra finch 
Hatching failure is a surprisingly common phenomenon given that natural selection constantly works against it. In birds, an average of about 10 per cent of eggs across species fail to hatch, often owing to the death of embryos. While embryo mortality owing to inbreeding is both well-documented and evolutionarily plausible, this is not true for other sources of mortality. In fact, the basis for hatching failure in natural populations remains largely unexplained. Here, we demonstrate that embryo mortality in captive zebra finches (Taeniopygia guttata) follows from chromosomal aneuploidy or polyploidy. As part of microsatellite genotyping of a captive breeding population, we found 12 individuals (3.6%) with three alleles among 331 embryos that had died during development, while there were no such cases observed among 1210 adult birds. Subsequent genotyping of 1920 single nucleotide polymorphism markers distributed across the genome in birds with three alleles at microsatellite loci, and in greater than 1000 normal birds, revealed that the aberrant karyotypes involved cases of both trisomies and triploidy. Cases of both maternally and paternally inherited trisomies resulted from non-disjunction during meiosis. Maternally inherited cases of triploidy were attributable to failure of meiosis leading to diploid eggs, while paternally inherited triploidy could have arisen either from diploid sperm or from dispermy. Our initial microsatellite screening set only had the power to detect less than 10 per cent of trisomies and by extrapolation, our data therefore tentatively suggest that trisomy might be a major cause of embryo mortality in zebra finches.
doi:10.1098/rspb.2010.0394
PMCID: PMC2982043  PMID: 20444723
chromosomal anomalities; diploid sperm; meiotic error; non-disjunction; polyploidy; polyspermy
5.  Do Zebra Finch Parents Fail to Recognise Their Own Offspring? 
PLoS ONE  2011;6(4):e18466.
Individual recognition systems require the sender to be individually distinctive and the receiver to be able to perceive differences between individuals and react accordingly. Many studies have demonstrated that acoustic signals of almost any species contain individualized information. However, fewer studies have tested experimentally if those signals are used for individual recognition by potential receivers. While laboratory studies using zebra finches have shown that fledglings recognize their parents by their “distance call”, mutual recognition using the same call type has not been demonstrated yet. In a laboratory study with zebra finches, we first quantified between-individual acoustic variation in distance calls of fledglings. In a second step, we tested recognition of fledgling calls by parents using playback experiments. With a discriminant function analysis, we show that individuals are highly distinctive and most measured parameters show very high potential to encode for individuality. The response pattern of zebra finch parents shows that they do react to calls of fledglings, however they do not distinguish between own and unfamiliar offspring, despite individual distinctiveness. This finding is interesting in light of the observation of a high percentage of misdirected feedings in our communal breeding aviaries. Our results demonstrate the importance of adopting a receiver's perspective and suggest that variation in fledgling contact calls might not be used in individual recognition of offspring.
doi:10.1371/journal.pone.0018466
PMCID: PMC3076377  PMID: 21533233
6.  Cryptic multiple hypotheses testing in linear models: overestimated effect sizes and the winner's curse 
Fitting generalised linear models (GLMs) with more than one predictor has become the standard method of analysis in evolutionary and behavioural research. Often, GLMs are used for exploratory data analysis, where one starts with a complex full model including interaction terms and then simplifies by removing non-significant terms. While this approach can be useful, it is problematic if significant effects are interpreted as if they arose from a single a priori hypothesis test. This is because model selection involves cryptic multiple hypothesis testing, a fact that has only rarely been acknowledged or quantified. We show that the probability of finding at least one ‘significant’ effect is high, even if all null hypotheses are true (e.g. 40% when starting with four predictors and their two-way interactions). This probability is close to theoretical expectations when the sample size (N) is large relative to the number of predictors including interactions (k). In contrast, type I error rates strongly exceed even those expectations when model simplification is applied to models that are over-fitted before simplification (low N/k ratio). The increase in false-positive results arises primarily from an overestimation of effect sizes among significant predictors, leading to upward-biased effect sizes that often cannot be reproduced in follow-up studies (‘the winner's curse’). Despite having their own problems, full model tests and P value adjustments can be used as a guide to how frequently type I errors arise by sampling variation alone. We favour the presentation of full models, since they best reflect the range of predictors investigated and ensure a balanced representation also of non-significant results.
doi:10.1007/s00265-010-1038-5
PMCID: PMC3015194  PMID: 21297852
Bonferroni correction; Effect size estimation; Generalised linear models; Model selection; Multiple regression; Multiple testing; Parameter estimation; Publication bias
7.  Compensatory investment in zebra finches: females lay larger eggs when paired to sexually unattractive males 
The classical version of the differential allocation hypothesis states that, when females reproduce over their lifetime with partners that differ in their genetic quality, they should invest more in reproduction with high-quality males. However, in species with lifetime monogamy, such as the zebra finch, partner quality will typically remain the same. In this case, the compensatory investment (CI) hypothesis predicts higher investment for low-quality males, because low genetic quality offspring are more dependent on maternal resources. Here, we show that female zebra finches invested more resources, both in terms of egg volume and yolk carotenoid content, when paired to a low genetic quality male, as judged from his previous ability to obtain extra-pair paternity in aviary colonies. We also found that females deposited slightly larger amounts of testosterone into eggs when paired to a low parental quality male, as judging from his previous success in rearing offspring. This is, to our knowledge, the first experimental support for the CI hypothesis in a species with lifetime monogamy. We stress that in more promiscuous species, the benefits of classical differential allocation may partly be neutralized by the supposed benefits of CI.
doi:10.1098/rspb.2008.1251
PMCID: PMC2660937  PMID: 18986974
carotenoids; differential allocation hypothesis; egg resources; mate attractiveness; maternal effects; reproductive investment
8.  Conclusions beyond support: overconfident estimates in mixed models 
Behavioral Ecology  2008;20(2):416-420.
Mixed-effect models are frequently used to control for the nonindependence of data points, for example, when repeated measures from the same individuals are available. The aim of these models is often to estimate fixed effects and to test their significance. This is usually done by including random intercepts, that is, intercepts that are allowed to vary between individuals. The widespread belief is that this controls for all types of pseudoreplication within individuals. Here we show that this is not the case, if the aim is to estimate effects that vary within individuals and individuals differ in their response to these effects. In these cases, random intercept models give overconfident estimates leading to conclusions that are not supported by the data. By allowing individuals to differ in the slopes of their responses, it is possible to account for the nonindependence of data points that pseudoreplicate slope information. Such random slope models give appropriate standard errors and are easily implemented in standard statistical software. Because random slope models are not always used where they are essential, we suspect that many published findings have too narrow confidence intervals and a substantially inflated type I error rate. Besides reducing type I errors, random slope models have the potential to reduce residual variance by accounting for between-individual variation in slopes, which makes it easier to detect treatment effects that are applied between individuals, hence reducing type II errors as well.
doi:10.1093/beheco/arn145
PMCID: PMC2657178  PMID: 19461866
experimental design; maternal effects; mixed-effect models; random regression; repeated measures; type I error
9.  Do Individual Females Differ Intrinsically in Their Propensity to Engage in Extra-Pair Copulations? 
PLoS ONE  2007;2(9):e952.
Background
While many studies have investigated the occurrence of extra-pair paternity in wild populations of birds, we still know surprisingly little about whether individual females differ intrinsically in their principal readiness to copulate, and to what extent this readiness is affected by male attractiveness.
Methodology/Findings
To address this question I used captive zebra finches (Taeniopygia guttata) as a model system. I first measured female readiness to copulate when courted by a male for the first time in life. Second, I conducted choice-chamber experiments to assess the mating preferences of individual females prior to pair formation. I then paired females socially with a non-desired mate and once they had formed a stable pair bond, I observed the inclination of these females to engage in extra-pair copulations with various males. Females showing a high readiness to copulate when courted by a male for the first time in life were much more likely to engage in extra-pair copulations later in life than others. Male attractiveness, as measured in choice tests, was a useful predictor of whether females engaged in extra-pair copulations with these males, but, surprisingly, the attractiveness of a female's social partner had no effect on her fidelity. However, it remained unclear what made some males more attractive than others. Contrary to a widespread but rarely tested hypothesis, females did not preferentially copulate with males having a redder beak or singing at a higher rate. Rather it seemed that song rate was a confounding factor in choice-chamber experiments: song attracted the female's attention but did not increase the male's attractiveness as a copulation partner.
Conclusions/Significance
Intrinsic variation in female readiness to copulate as well as variation in the attractiveness of the extra-pair male but not the social partner decided the outcome of extra-pair encounters.
doi:10.1371/journal.pone.0000952
PMCID: PMC1978515  PMID: 17895992
10.  Quantitative genetics and behavioural correlates of digit ratio in the zebra finch 
A recent study on a captive zebra finch population suggested that variation in digit ratio (i.e. the relative length of the second to the fourth toe) might be an indicator of the action of sex steroids during embryo development, as is widely assumed for human digits. Zebra finch digit ratio was found to vary with offspring sex, laying order of eggs within a clutch, and to predict aspects of female mating behaviour. Hence, it was proposed that the measurement of digit ratio would give insights into how an individual's behaviour is shaped by its maternal environment. Studying 500 individuals of a different zebra finch population I set out to: (1) determine the proximate causes of variation in digit ratio by means of quantitative genetics and (2) to search for phenotypic and genetic correlations between digit ratio, sexual behaviour and aspects of fitness. In contrast to the earlier study, I found no sexual dimorphism in digit ratio and no effect of either laying order or experimentally altered hatching order on digit ratio. Instead, I found that variation in digit ratio was almost entirely additive genetic, with heritability estimates ranging from 71 to 84%. The rearing environment (from egg deposition to independence) explained an additional 5–6% of the variation in digit ratio, but there was no indication of any maternal effects transmitted through the egg. I found highly significant phenotypic correlations (and genetic correlations of similar size) between digit ratio and male song rate (positive correlation) as well as between digit ratio and female hopping activity in a choice chamber (negative correlation). Rather surprisingly, the strength of these correlations differed significantly between subsequent generations of the same population, illustrating how quickly such correlations can appear and disappear probably due to genotype–environment interactions.
doi:10.1098/rspb.2005.3264
PMCID: PMC1559980  PMID: 16321787
genetic correlation; genotype–environment interaction; heritability; maternal environment; mating behaviour; morphology
11.  A novel song parameter correlates with extra-pair paternity and reflects male longevity. 
Although elaborate bird song provides one of the prime examples of a trait that evolved under sexual selection, it is still unclear whether females judge the quality of males by attributes of their song and whether these song features honestly signal a male's genetic quality. We measured the ability of male dusky warblers Phylloscopus fuscatus to maintain a high sound amplitude during singing, which probably reflects an individual's physiological limitations. This new measure of singing performance was correlated with male longevity and with extra-pair paternity, indicating that females who copulated with better singers obtained 'good genes' for their offspring. Our findings are consistent with the idea that females assess male quality by subtle differences in their performance during the production of notes, rather than by the quantity or versatility of song. In addition, observations on territorial conflicts indicate that attractive males invest less in competition over territories because they can reproduce via extra-pair paternity.
doi:10.1098/rspb.2002.2039
PMCID: PMC1691048  PMID: 12137578
12.  HERITABILITY OF AND EARLY ENVIRONMENT EFFECTS ON VARIATION IN MATING PREFERENCES 
Many species show substantial between-individual variation in mating preferences, but studying the causes of such variation remains a challenge. For example, the relative importance of heritable variation versus shared early environment effects (like sexual imprinting) on mating preferences has never been quantified in a population of animals. Here, we estimate the heritability of and early rearing effects on mate choice decisions in zebra finches based on the similarity of choices between pairs of genetic sisters raised apart and pairs of unrelated foster sisters. We found a low and nonsignificant heritability of preferences and no significant shared early rearing effects. A literature review shows that a low heritability of preferences is rather typical, whereas empirical tests for the relevance of sexual imprinting within populations are currently limited to very few studies. Although effects on preference functions (i.e., which male to prefer) were weak, we found strong individual consistency in choice behavior and part of this variation was heritable. It seems likely that variation in choice behavior (choosiness, responsiveness, sampling behavior) would produce patterns of nonrandom mating and this might be the more important source of between-individual differences in mating patterns.
doi:10.1111/j.1558-5646.2009.00890.x
PMCID: PMC2871178  PMID: 19895552
Heritability; mate choice; preference functions; quantitative genetics; sexual imprinting; zebra finch

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