Testing the phenotype-linked fertility hypothesis in the presence and absence of inbreeding.

The phenotype-linked fertility hypothesis suggests that females can judge male fertility by inspecting male phenotypic traits. This is because male sexually selected traits might correlate with sperm quality if both are sensitive to factors that influence male condition. A recent meta-analysis found little support for this hypothesis, suggesting little or no shared condition dependence. However, we recently reported that in captive zebra finches (Taeniopygia guttata) inbreeding had detrimental effects both on phenotypic traits and on measures of sperm quality, implying that variation in inbreeding could induce positive covariance between indicator traits and sperm quality. Therefore, we here assess empirically the average strength of correlations between phenotypic traits (courtship rate, beak colour, tarsus length) and measures of sperm quality (proportion of functional sperm, sperm velocity, sperm length) in populations of only outbred individuals and in mixed populations consisting of inbreds (F = 0.25) and outbreds (F = 0). As expected, phenotype sperm-trait correlations were stronger when the population contained a mix of inbred and outbred individuals. We also found unexpected heterogeneity between our two study populations, with correlations being considerably stronger in a domesticated population than in a recently wild-derived population. Correlations ranged from essentially zero among outbred-only wild-derived birds (mean Fisher's Zr ± SE = 0.03 ± 0.10) to moderately strong among domesticated birds of mixed inbreeding status (Zr ± SE = 0.38 ± 0.08). Our results suggest that, under some conditions, the phenotype-linked fertility hypothesis might apply.

Meiotic recombination shapes precision of pedigree- and marker-based estimates of inbreeding.

The proportion of an individual's genome that is identical by descent (GWIBD) can be estimated from pedigrees (inbreeding coefficient 'Pedigree F') or molecular markers ('Marker F'), but both estimators come with error. Assuming unrelated pedigree founders, Pedigree F is the expected proportion of GWIBD given a specific inbreeding constellation. Meiotic recombination introduces variation around that expectation (Mendelian noise) and related pedigree founders systematically bias Pedigree F downward. Marker F is an estimate of the actual proportion of GWIBD but it suffers from the sampling error of markers plus the error that occurs when a marker is homozygous without reflecting common ancestry (identical by state). We here show via simulation of a zebra finch and a human linkage map that three aspects of meiotic recombination (independent assortment of chromosomes, number of crossovers and their distribution along chromosomes) contribute to variation in GWIBD and thus the precision of Pedigree and Marker F. In zebra finches, where the genome contains large blocks that are rarely broken up by recombination, the Mendelian noise was large (nearly twofold larger s.d. values compared with humans) and Pedigree F thus less precise than in humans, where crossovers are distributed more uniformly along chromosomes. Effects of meiotic recombination on Marker F were reversed, such that the same number of molecular markers yielded more precise estimates of GWIBD in zebra finches than in humans. As a consequence, in species inheriting large blocks that rarely recombine, even small numbers of microsatellite markers will often be more informative about inbreeding and fitness than large pedigrees.

Quantifying realized inbreeding in wild and captive animal populations.

Most molecular measures of inbreeding do not measure inbreeding at the scale that is most relevant for understanding inbreeding depression-namely the proportion of the genome that is identical-by-descent (IBD). The inbreeding coefficient FPed obtained from pedigrees is a valuable estimator of IBD, but pedigrees are not always available, and cannot capture inbreeding loops that reach back in time further than the pedigree. We here propose a molecular approach to quantify the realized proportion of the genome that is IBD (propIBD), and we apply this method to a wild and a captive population of zebra finches (Taeniopygia guttata). In each of 948 wild and 1057 captive individuals we analyzed available single-nucleotide polymorphism (SNP) data (260 SNPs) spread over four different genomic regions in each population. This allowed us to determine whether any of these four regions was completely homozygous within an individual, which indicates IBD with high confidence. In the highly nomadic wild population, we did not find a single case of IBD, implying that inbreeding must be extremely rare (propIBD=0-0.00094, 95% CI). In the captive population, a five-generation pedigree strongly underestimated the average amount of realized inbreeding (FPed=0.013

Basal metabolic rate can evolve independently of morphological and behavioural traits.

Quantitative genetic analyses of basal metabolic rate (BMR) can inform us about the evolvability of the trait by providing estimates of heritability, and also of genetic correlations with other traits that may constrain the ability of BMR to respond to selection. Here, we studied a captive population of zebra finches (Taeniopygia guttata) in which selection lines for male courtship rate have been established. We measure BMR in these lines to see whether selection on male sexual activity would change BMR as a potentially correlated trait. We find that the genetic correlation between courtship rate and BMR is practically zero, indicating that the two traits can evolve independently of each other. Interestingly, we find that the heritability of BMR in our population (h(2)=0.45) is markedly higher than was previously reported for a captive zebra finch population from Norway. A comparison of the two studies shows that additive genetic variance in BMR has been largely depleted in the Norwegian population, especially the genetic variance in BMR that is independent of body mass. In our population, the slope of BMR increase with body mass differs not only between the sexes but also between the six selection lines, which we tentatively attribute to genetic drift and/or founder effects being strong in small populations. Our study therefore highlights two things. First, the evolvability of BMR may be less constrained by genetic correlations and lack of independent genetic variation than previously described. Second, genetic drift in small populations can rapidly lead to different evolvabilities across populations.

No heightened condition dependence of zebra finch ornaments--a quantitative genetic approach.

The developmental stress hypothesis offers a mechanism to maintain honesty of sexually selected ornaments, because only high quality individuals will be able to develop full ornamentation in the face of stress during early development. Experimental tests of this hypothesis have traditionally involved the manipulation of one aspect of the rearing conditions and an examination of effects on adult traits. Here, we instead use a statistically powerful quantitative genetic approach to detect condition dependence. We use animal models to estimate environmental correlations between a measure of early growth and adult traits. This way, we could make use of the sometimes dramatic differences in early growth of more than 800 individually cross-fostered birds and measure the effect on a total of 23 different traits after birds reached maturity. We find strong effects of environmental growth conditions on adult body size, body mass and fat deposition, moderate effects on beak colour in both sexes, but no effect on song and plumage characters. Rather surprisingly, there was no effect on male attractiveness, both measured in mate choice trials and under socially complex conditions in aviaries. There was a trend for a positive effect of good growth conditions on the success at fertilizing eggs in males breeding in aviaries whereas longevity was not affected in either sex. We conclude that zebra finches are remarkably resilient to food shortage during growth and can compensate for poor growth conditions without much apparent life-history trade-offs. Our results do not support the hypothesis that sexually selected traits show heightened condition dependence compared to nonsexually selected traits.

Sexual imprinting on continuous variation: do female zebra finches prefer or avoid unfamiliar sons of their foster parents?

Sexual imprinting on discrete variation that serves the identification of species, morphs or sexes is well documented. By contrast, sexual imprinting on continuous variation leading to individual differences in mating preferences within a single species, morph and sex has been studied only once (in humans). We measured female preferences in a captive population of wild-type zebra finches. Individual cross-fostering ensured that all subjects grew up with unrelated foster parents and nest mates. Females from two cohorts (N = 113) were given a simultaneous choice between (two or four) unfamiliar males, one of which was a genetic son of their foster parents (SFP). We found no significant overall preference for the SFP (combined effect size d = 0.14 +/- 0.15). Additionally, we tested if foster parent traits could potentially explain between-female variation in preferences. However, neither the effectiveness of cooperation between the parents nor male contribution to parental care affected female preferences for the son of the foster father. We conclude that at least in zebra finches sexual imprinting is not a major source of between-individual variation in mating preferences.

Bill morphology reflects female independence from male parental help.

The study of territorial polygyny in birds has been influential in the development of the theory of social mating systems. Alternative female mating options have been studied within the framework of the polygyny-threshold model and later as the outcome of conflicts of interest between individuals. However, little attention has been given to variations between individual females, and how this affects their mating behaviour. Here, we test the hypothesis that some females are better adapted to raise nestlings without male assistance, and thus to mate polygynously. Specifically, we investigate whether intraspecific variation in female bill morphology is related to mating behaviour. This hypothesis is derived from earlier studies showing that, in both intra- and interspecific comparisons, uniparental care by females is correlated with the catching of larger prey items than when both parents provision the young. Using the polygynous dusky warbler (Phylloscopus fuscatus) as a model species, we found that, in accordance with our prediction, females with deep bills were more likely to mate as a secondary female. Moreover, regardless of mating status, females with deep bills settled in territories with more food and they received less male assistance in feeding their offspring. We argue that females with stronger bills are better adapted to exploit the abundance of large food items in rich territories and thus to raise young on their own. Our results demonstrate the importance of studying variations between individual females, and provide evidence for an extended version of the 'constrained-female hypothesis'. As bill depth is a highly heritable trait, our study strongly suggests that variation in female mating behaviour is not only related to ecological factors and female condition (as shown elsewhere) but also to heritable morphological traits.