Basal metabolic rate can evolve independently of morphological and behavioural traits

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

Heritability of corticosterone response and changes in life history traits during selection in the zebra finch

Vertebrates respond to environmental stressors through the neuro-endocrine stress response, which involves the production of glucocorticoids. We have selected independent, duplicate divergent lines of zebra finches for high, low and control corticosterone responses to a mild stressor. This experiment has shown that over the first four generations, the high lines have demonstrated a significant realized heritability of about 20%. However, the low lines have apparently not changed significantly from controls. This asymmetry in response is potentially because of the fact that all birds appear to be showing increased adaptation to the environment in which they are housed, with significant declines in corticosterone response in control lines as well as low lines. Despite the existence of two- to threefold difference in mean corticosterone titre between high and low lines, there were no observed differences in testosterone titre in adult male birds from the different groups. In addition, there were no consistent, significant differences between the lines in any of the life history variables measured--number of eggs laid per clutch, number of clutches or broods produced per pair, number of fledglings produced per breeding attempt, nor in any of egg, nestling and fledgling mortality. These results highlight the fact that the mechanisms that underlie variation in the avian physiological system can be modified to respond to differences between environments through selection. This adds an additional level of flexibility to the avian physiological system, which will allow it to respond to environmental circumstances.     

Sex allocation in response to paternal attractiveness in the zebra finch

Females mated to attractive males are predicted to produce male-biasedbroods. Previous studies on zebra finches, Taeniopygia guttata,in which colored leg rings were used to alter male attractiveness,support this hypothesis. However, because molecular sexing techniqueswere not available, it was not known when during developmentthis bias arose. Also, because both attractive (red-ringed)and unattractive (green-ringed) males were within the same aviary,assortative mating between treatments may have confounded theresults. Using two different experimental designs, we testedwhether the sex ratio of zebra finch eggs and chicks differedin response to paternal ring color whilst controlling for assortativemating between treatments. In the aviary experiment, birds couldinteract socially, but all males in an aviary had the same legring color. In the cage experiment, each female was randomlyassigned a red- or green-ringed mate, thus also eliminatingassortative mating within treatments. Offspring were sexed basedon plumage or using a molecular method. The sex ratio at layingdid not differ between treatments in either the aviary (n =313 eggs) or cage (n = 151 eggs) experiments, suggesting thatfemale zebra finches do not manipulate the primary sex ratioin response to their mate's ring color. However, in the cageexperiment we found greater male embryonic mortality in theattractive group, which resulted in a female-biased sex ratioat sexual maturity, that is, in the opposite direction to thatfound in previous studies. Possible explanations for the disparitybetween our results and those of previous studies are considered.     

QTL and quantitative genetic analysis of beak morphology reveals patterns of standing genetic variation in an Estrildid finch

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.     

成年斑胸草雀在体HVC-RA突触传递的电生理特性

鸣禽高级发声中枢（high vocal center,HVC）至弓状皮质栎核（robust nucleus ofthe arcopallium,RA）的突触传递是鸣唱运动通路中的关键部分.本文运用在体场电位电生理记录的方法,研究了成年雄性斑胸草雀（Taeniopygia guttata）HVC-RA突触的电生理特性.实验结果显示,刺激HVC,在RA内所记录到的诱发场电位幅度较小.配对脉冲检测发现,HVC-RA突触传递具有明显的配对脉冲易化特性.当以强直刺激作用于HVC,RA内诱发场电位随即显著减小,并在15 min内逐渐恢复,表明HVC-RA突触传递在强直刺激过后出现了短时抑制.该通路的突触传递特性可能与其在发声控制中的作用有关.以上的实验结果为进一步研究发声运动过程中的突触可塑性提供了资料.     

Distribution and developmental change in [3H]MK-801 binding within zebra finch song nuclei

In many songbirds, vocal learning depends upon appropriate auditory experience during a sensitive period that coincides with the formation and reorganization of song-related neural pathways. Because some effects of early sensory experience on neural organization and early learning have been linked to activation of N-methyl-d-aspartate (NMDA) receptors, we measured binding to this receptor within the neural system controlling song behavior in zebra finches. Quantitative autoradiography was used to measure binding of the noncompetitive antagonist [³H]MK-801 (dizocilpine) in the brains of both adult and juvenile male zebra finches, focusing on four telencephalic regions implicated in song learning and production. Overall, the pattern of MK-801 binding in zebra finches was similar to the pattern found in rats (Monaghan and Cotman, 1985, J. Neurosci. 5:2909–2919; Sakurai, Cha, Penney, and Young, 1991, Neuroscience 40:533–543). That is, binding was highest in the telencephalon, intermediate in thalamic regions, and virtually absent from the brain stem and cerebellum. The telencephalic song areas exhibited intermediate levels of binding, and binding in the juveniles was not significantly different from adult levels in most song nuclei. However, in the lateral magnocellular nucleus of the anterior neostriatum (IMAN), binding at 30 days of age was significantly higher than binding in adults. Given the established role of NMDA receptors in other developing neural systems, both their presence in song control nuclei and their developmental regulation within a region implicated in song learning suggest that NMDA receptors play a role in mediating effects of auditory experience on the development of song behavior.     

Sex-specific patterns of yolk androgen allocation depend on maternal diet in the zebra finch

Females are predicted to adjust their reproductive investmentin relation to resource quality. In zebra finches (Taeniopygiaguttata), diet quality has been found to influence egg massboth between and within clutches. We tested the prediction thatdiet quality also affects the quantity of maternally allocatedyolk testosterone and 5-dihydrotestosterone (DHT) between andwithin clutches. We also investigated whether this pattern differedbetween male and female eggs. Females laid eggs on a high-quality(HQ) or a low-quality (LQ) diet. Eggs were removed at layingand artificially incubated for 72 h, after which time embryoswere sexed and yolk androgens assayed. Diet treatments werethen swapped and the experiment repeated. Because there wasevidence of a carry-over effect between breeding rounds, webased our conclusions mainly on the results from the first breedinground. On the HQ diet, but not on the LQ diet, infertile eggscontained more testosterone than did fertile eggs in round one.Although there were no overall differences in within-clutchpatterns of androgen deposition between the diets, this changedwhen embryo sex was taken into account. On the HQ diet, testosteronedecreased with laying sequence for male eggs but increased withlaying sequence for female eggs. On the LQ diet, mothers' maleeggs contained more testosterone and DHT than did female eggsregardless of position in the laying sequence. Our data suggestthat there are complex, context-dependent mechanisms of sex-specificandrogen allocation in this species.     

Costly steroids: egg testosterone modulates nestling metabolic rate in the zebra finch

The transfer of non-genetic resources from mother to the offspring often has considerable consequences for offspring performance. In birds, maternally derived hormones are known to influence a variety of morphological, physiological and behavioural traits in the chick. So far, the range of these hormonal effects involves benefits in terms of enhanced growth and competitive ability as well as costs in terms of immunosuppression. However, since yolk hormones can enhance growth and begging activity, high levels of these hormones may also involve energetic costs. Here, we show experimentally that elevated levels of prenatal testosterone increase resting metabolic rate in nestling zebra finches (Taeniopygia guttata). Surprisingly, however, elevation of prenatal testosterone did not result in higher growth rates and, thus, differences in resting metabolism do not seem to be linked to nestling growth. We conclude that apart from immunosuppressive effects, high levels of egg steroids may also entail costs in terms of increased energy expenditure.     

Horizontal transmission of the father's song in the zebra finch (Taeniopygia guttata)

As is the case for human speech, birdsong is transmitted across generations by imitative learning. Although transfer of song patterns from adults to juveniles typically occurs via vertical or oblique transmission, there is also evidence of horizontal transmission between juveniles of the same generation. Here, we show that a young male zebra finch (Taeniopygia guttata) that has been exposed to its father during the sensitive period for song learning can lead a brother, that has never heard the paternal song, to imitate some sounds of the father. Moreover, song similarity between the two brothers was higher than the similarity measured between the paternal song and the song of the brother that had a week-long exposure to the father. We speculate that the phenomenon of within-generation song learning among juveniles may be more widespread than previously thought and that when a juvenile evaluates potential models for imitative learning, a sibling may be as salient as an adult.     

Mitochondrial haplotype does not affect sperm velocity in the zebra finch Taeniopygia guttata

Mitochondrial DNA (mtDNA) variation has been suggested as a possible cause of variation in male fertility because sperm activity is tightly coupled to mitochondrial oxidative phosphorylation and ATP production, both of which are sensitive to mtDNA mutations. Since male‐specific phenotypes such as sperm have no fitness consequences for mitochondria due to maternal mitochondrial (and mtDNA) inheritance, mtDNA mutations that are deleterious in males but which have negligible or no fitness effect in females can persist in populations. How often such mutations arise and persist is virtually unknown. To test whether there were associations between mtDNA variation and sperm performance, we haplotyped 250 zebra finches Taeniopygia guttata from a large pedigreed‐population and measured sperm velocity using computer‐assisted sperm analysis. Using quantitative genetic ‘animal’ models, we found no effect of mtDNA haplotype on sperm velocity. Therefore, there is no evidence that in this system mitochondrial mutations have asymmetric fitness effects on males and females, leading to genetic variation in male fertility that is blind to natural selection.     

Acetylcholinesterase in central vocal control nuclei of the zebra finch (<Emphasis Type=Italic>Taeniopygia guttata</Emphasis>)

The distribution of acetylcholinesterase (AChE) in the central vocal control nuclei of the zebra finch was studied using enzyme histochemistry. AChE fibres and cells are intensely labelled in the forebrain nucleus area X, strongly labelled in high vocal centre (HVC) perikarya, and moderately to lightly labelled in the somata and neuropil of vocal control nuclei robust nucleus of arcopallium (RA), medial magnocellular nucleus of the anterior nidopallium (MMAN) and lateral magnocellular nucleus of the anterior nidopallium (LMAN). The identified sites of cholinergic and/or cholinoceptive neurons are similar to the cholinergic presence in vocal control regions of other songbirds such as the song sparrow, starling and another genus of the zebra finch (Poephila guttata), and to a certain extent in parallel vocal control regions in vocalizing birds such as the budgerigar. AChE presence in the vocal control system suggests innervation by either afferent projecting cholinergic systems and/or local circuit cholinergic neurons. Co-occurrence with choline acetyltransferase (ChAT) indicates efferent cholinergic projections. The cholinergic presence in parts of the zebra finch vocal control system, such as the area X, that is also intricately wired with parts of the basal ganglia, the descending fibre tracts and brain stem nuclei could underlie this circuitry’s involvement in sensory processing and motor control of song.     

Understanding and using quantitative genetic variation

Quantitative genetics, or the genetics of complex traits, is the study of those characters which are not affected by the action of just a few major genes. Its basis is in statistical models and methodology, albeit based on many strong assumptions. While these are formally unrealistic, methods work. Analyses using dense molecular markers are greatly increasing information about the architecture of these traits, but while some genes of large effect are found, even many dozens of genes do not explain all the variation. Hence, new methods of prediction of merit in breeding programmes are again based on essentially numerical methods, but incorporating genomic information. Long-term selection responses are revealed in laboratory selection experiments, and prospects for continued genetic improvement are high. There is extensive genetic variation in natural populations, but better estimates of covariances among multiple traits and their relation to fitness are needed. Methods based on summary statistics and predictions rather than at the individual gene level seem likely to prevail for some time yet.     

Repeatability and heritability of reproductive traits in free-ranging snakes

The underlying genetic basis of life-history traits in free-ranging animals is critical to the effects of selection on such traits, but logistical constraints mean that such data are rarely available. Our long-term ecological studies on free-ranging oviparous snakes (keelbacks, Tropidonophis mairii (Gray, 1841), Colubridae) on an Australian floodplain provide the first such data for any tropical reptile. All size-corrected reproductive traits (egg mass, clutch size, clutch mass and post-partum maternal mass) were moderately repeatable between pairs of clutches produced by 69 female snakes after intervals of 49-1152 days, perhaps because maternal body condition was similar between clutches. Parent-offspring regression of reproductive traits of 59 pairs of mothers and daughters revealed high heritability for egg mass (h2= 0.73, SE=0.24), whereas heritability for the other three traits was low (< 0.37). The estimated heritability of egg mass may be inflated by maternal effects such as differential allocation of yolk steroids to different-sized eggs. High heritability of egg size may be maintained (rather than eroded by stabilizing selection) because selection acts on a trait (hatchling size) that is determined by the interaction between egg size and incubation substrate rather than by egg size alone. Variation in clutch size was mainly because of environmental factors (h2=0.04), indicating that one component of the trade-off between egg size and clutch size is under much tighter genetic control than the other. Thus, the phenotypic trade-off between egg size and egg number in keelback snakes occurs because each female snake must allocate a finite amount of energy into eggs of a genetically determined size.     

Condition-dependent sexual traits and social dominance in the house finch

Elaboration of costly sexual traits can reduce investment inother aspects of reproduction, such as parental care or intrasexualcompetition, which may lead to the evolution of alternativemating tactics. In house finches (Carpodacus mexicanus), lesselaborately ornamented (dull) males tend to dominate more elaborated(redder) males, but redder males pair earlier and invest morein parental care. This suggests that males may pursue alternativeparental or competitive tactics, depending on the elaborationof their sexual trait. Elevation of testosterone, a hormonethat is closely associated with condition in male house finches,influences dominance and sexual behaviors but is antagonisticto parental behaviors. We tested the hypothesis that the higherdominance status of dull males reflects an alternative testosterone-dependentmating tactic. First, we experimentally manipulated the testosteronelevels of captive males and measured the effect on dominancerank, and second, we measured the association of testosteroneelevation and plumage hue in free-living males. We found that,as predicted, testosterone elevation increased dominance rankin captive males. However, in free-living males, testosteronelevels were higher in redder males, suggesting that testosteroneis dissociated from dominance status under natural circumstances.This may be because the context of social interactions and thehigher motivation of dull males to access food resources havea stronger influence on the outcome of dominance interactionsthan does the physiological effects of testosterone elevation.In turn, the strong positive correlation between testosteronelevels and plumage elaboration likely reflects the common conditiondependence of these traits.