Song in the cold is 'hot': memory of and preference for sexual signals perceived under thermal challenge

The environmental conditions under which signals are perceived can affect receiver responses. Many songbird populations produce a song chorus at dawn, when, in cold habitats, they would experience thermal challenge. We recorded temperature and the song activity of Lincoln's sparrows (Melospiza lincolnii) on a high-elevation meadow, and determined that song behaviour is concentrated around the coldest time of the day, at dawn. We hypothesized that this is because male song in the cold is more attractive to females than song in the warm. To test this, we exposed laboratory-housed Lincoln's sparrow females to songs at 1°C and 16°C, which they naturally experience in the wild. Females spent 40 per cent more time close to the speaker during playback at 1°C than at 16°C. When tested at 16°C 1-2 days later, females biased their movement towards the speaker playing songs previously heard at 1°C over 16°C. Thus, female Lincoln's sparrows remembered and affiliated with songs they heard under thermal challenge, indicating that the thermal environment can affect the attractiveness of a sexual signal.     

Effects of spontaneous mutation accumulation on sex ratio traits in a parasitoid wasp

Sex allocation theory has proved extremely successful at predicting when individuals should adjust the sex of their offspring in response to environmental conditions. However, we know rather little about the underlying genetics of sex ratio or how genetic architecture might constrain adaptive sex-ratio behavior. We examined how mutation influenced genetic variation in the sex ratios produced by the parasitoid wasp Nasonia vitripennis. In a mutation accumulation experiment, we determined the mutability of sex ratio, and compared this with the amount of genetic variation observed in natural populations. We found that the mutability (h(2)(m)) ranges from 0.001 to 0.002, similar to estimates for life-history traits in other organisms. These estimates suggest one mutation every 5-60 generations, which shift the sex ratio by approximately 0.01 (proportion males). In this and other studies, the genetic variation in N. vitripennis sex ratio ranged from 0.02 to 0.17 (broad-sense heritability, H(2)). If sex ratio is maintained by mutation-selection balance, a higher genetic variance would be expected given our mutational parameters. Instead, the observed genetic variance perhaps suggests additional selection against sex-ratio mutations with deleterious effects on other fitness traits as well as sex ratio (i.e., pleiotropy), as has been argued to be the case more generally.     

Phenotypic variation and covariation indicate high evolvability of acoustic communication in crickets

Studying the genetic architecture of sexual traits provides insight into the rate and direction at which traits can respond to selection. Traits associated with few loci and limited genetic and phenotypic constraints tend to evolve at high rates typically observed for secondary sexual characters. Here, we examined the genetic architecture of song traits and female song preferences in the field crickets Gryllus rubens and Gryllus texensis. Song and preference data were collected from both species and interspecific F1 and F2 hybrids. We first analysed phenotypic variation to examine interspecific differentiation and trait distributions in parental and hybrid generations. Then, the relative contribution of additive and additive‐dominance variation was estimated. Finally, phenotypic variance–covariance ( P ) matrices were estimated to evaluate the multivariate phenotype available for selection. Song traits and preferences had unimodal trait distributions, and hybrid offspring were intermediate with respect to the parents. We uncovered additive and dominance variation in song traits and preferences. For two song traits, we found evidence for X‐linked inheritance. On the one hand, the observed genetic architecture does not suggest rapid divergence, although sex linkage may have allowed for somewhat higher evolutionary rates. On the other hand, P matrices revealed that multivariate variation in song traits aligned with major dimensions in song preferences, suggesting a strong selection response. We also found strong covariance between the main traits that are sexually selected and traits that are not directly selected by females, providing an explanation for the striking multivariate divergence in male calling songs despite limited divergence in female preferences.     

Fitness correlates of song repertoire size in free-living song sparrows (Melospiza melodia)

Models of sexual selection propose that exaggerated secondary sexual ornaments indicate a male's own fitness and the fitness of his offspring. These hypotheses have rarely been thoroughly tested in free-living individuals because overall fitness, as opposed to fitness components, is difficult to measure. We used 20 years of data from song sparrows (Melospiza melodia) inhabiting Mandarte Island, British Columbia, Canada, to test whether a male's song repertoire size, a secondary sexual trait, predicted overall measures of male or offspring fitness. Males with larger song repertoires contributed more independent and recruited offspring, and independent and recruited grandoffspring, to Mandarte's population. This was because these males lived longer and reared a greater proportion of hatched chicks to independence from parental care, not because females mated to males with larger repertoires laid or hatched more eggs. Furthermore, independent offspring of males with larger repertoires were more likely to recruit and then to leave more grandoffspring than were offspring of males with small repertoires. Although we cannot distinguish whether observed fitness variation reflected genetic or environmental effects on males or their offspring, these data suggest that female song sparrows would gain immediate and intergenerational fitness benefits by pairing with males with large song repertoires.     

Patterns and mechanisms of sex ratio distortion in the Collaborative Cross mouse mapping population

In species with single-locus, chromosome-based mechanisms of sex determination, the laws of segregation predict an equal ratio of females to males at birth. Here, we show that departures from this Mendelian expectation are commonplace in the 8-way recombinant inbred Collaborative Cross (CC) mouse population. More than one-third of CC strains exhibit significant sex ratio distortion (SRD) at wean, with twice as many male-biased than female-biased strains. We show that these pervasive sex biases persist across multiple breeding environments, are stable over time, and are not mediated by random maternal effects. SRD exhibits a heritable component, but QTL mapping analyses fail to nominate any large effect loci. These findings, combined with the reported absence of sex ratio biases in the CC founder strains, suggest that SRD manifests from multilocus combinations of alleles only uncovered in recombined CC genomes. We explore several potential complex genetic mechanisms for SRD, including allelic interactions leading to sex-biased lethality, genetic sex reversal, chromosome drive mediated by sex-linked selfish elements, and incompatibilities between specific maternal and paternal genotypes. We show that no one mechanism offers a singular explanation for this population-wide SRD. Instead, our data present preliminary evidence for the action of distinct mechanisms of SRD at play in different strains. Taken together, our work exposes the pervasiveness of SRD in the CC population and nominates the CC as a powerful resource for investigating diverse genetic causes of biased sex chromosome transmission.     

Sex-Ratio Meiotic Drive and Y-Linked Resistance in Drosophila affinis

Genetic elements that cheat Mendelian segregation by biasing transmission in their favor gain a significant fitness benefit. Several examples of sex-ratio meiotic drive, where one sex chromosome biases its own transmission at the cost of the opposite sex chromosome, exist in animals and plants. While the distorting sex chromosome gains a significant advantage by biasing sex ratio, the autosomes, and especially the opposite sex chromosome, experience strong selection to resist this transmission bias. In most well-studied sex-ratio meiotic drive systems, autosomal and/or Y-linked resistance has been identified. We specifically surveyed for Y-linked resistance to sex-ratio meiotic drive in Drosophila affinis by scoring the sex ratio of offspring sired by males with a driving X and one of several Y chromosomes. Two distinct types of resistance were identified: a restoration to 50/50 sex ratios and a complete reversal of sex ratio to all sons. We confirmed that fathers siring all sons lacked a Y chromosome, consistent with previously published work. Considerable variation in Y-chromosome morphology exists in D. affinis, but we showed that morphology does not appear to be associated with resistance to sex-ratio meiotic drive. We then used two X chromosomes (driving and standard) and three Y chromosomes (susceptible, resistant, and lacking) to examine fertility effects of all possible combinations. We find that both the driving X and resistant and lacking Y have significant fertility defects manifested in microscopic examination of testes and a 48-hr sperm depletion assay. Maintenance of variation in this sex-ratio meiotic drive system, including both the X-linked distorter and the Y-resistant effects, appear to be mediated by a complex interaction between fertility fitness and transmission dynamics.     

Quantitative genetic variance associated with chromosomal markers in segregating populations

Summary Use of chromosomal markers can accelerate genetic progress for quantitative traits in pedigree selection programs by providing early information on Mendelian segregation effects for individual progeny. Potential effectiveness of selection using markers is determined by the amount of additive genetic variance traced from parents to progeny by the markers. Theoretical equations for the amount of additive genetic variance associated with a marker were derived at the individual level and for a segregating population in joint linkage equilibrium. Factors considered were the number of quantitative trait loci linked to the marker, their individual effects, and recombination rates with the marker. Subsequently, the expected amount of genetic variance associated with a marker in a segregating population was derived. In pedigree selection programs in segregating populations, a considerable fraction of the genetic variance on a chromosome is expected to be associated with a marker located on that chromosome. For an average chromosome in the bovine, this fraction is approximately 40% of the Mendelian segregation variance contributed by the chromosome. The effects of interference and position of the marker on this expectation are relative small. Length of the chromosome has a large effect on the expected variance. Effectiveness of MAS is, however, greatly reduced by lack of polymorphism at the marker and inaccuracy of estimation of chromosome substitution effects. The size of the expected amount of genetic variance associated with a chromosomal marker indicates that, even when the marker is not the active locus, large chromosome substitution effects are not uncommon in segregating populations.     

Local adaptation within a hybrid species

Ecological divergence among populations may be strongly influenced by their genetic background. For instance, genetic admixture through introgressive hybridization or hybrid speciation is likely to affect the genetic variation and evolvability of phenotypic traits. We studied geographic variation in two beak dimensions and three other phenotypic traits of the Italian sparrow (Passer italiae), a young hybrid species formed through interbreeding between house sparrows (P. domesticus) and Spanish sparrows (P. hispaniolensis). We found that beak morphology was strongly influenced by precipitation regimes and that it appeared to be the target of divergent selection within Italian sparrows. Interestingly, however, the degree of parental genetic contribution in the hybrid species had no effect on phenotypic beak variation. Moreover, beak height divergence may mediate genetic differentiation between populations, consistent with isolation-by-adaptation within this hybrid species. The study illustrates how hybrid species may be relatively unconstrained by their admixed genetic background, allowing them to adapt rapidly to environmental variation.     

Indirect selection on female extra-pair reproduction? Comparing the additive genetic value of maternal half-sib extra-pair and within-pair offspring

One specific hypothesis explaining the evolution of extra-pair reproduction (EPR) by socially monogamous females is that EPR is under indirect selection because extra-pair offspring (EPO) sired by extra-pair males have higher additive genetic value for fitness than the within-pair offspring (WPO) a female would have produced had she solely mated with her socially paired male. This hypothesis has not been explicitly tested by comparing additive genetic value between EPO and the WPO they replaced. We show that the difference in additive genetic breeding value (BV) between EPO and the WPO they replaced is proportional to the genetic covariance between offspring fitness and male net paternity gain through EPR, and estimate this covariance with respect to offspring recruitment in free-living song sparrows (Melospiza melodia). Recruitment and net paternity gain showed non-zero additive genetic variance and heritability, and negative genetic covariance. Opposite to prediction, EPO therefore had lower BV for recruitment than the WPO they replaced. We thereby demonstrate an explicit quantitative genetic approach to testing the hypothesis that EPR allows polyandrous females to increase offspring additive genetic value, and suggest that there may be weak indirect selection against female EPR through reduced additive genetic value for recruitment of EPO versus WPO in song sparrows.     

Within-population variability in a moth sex pheromone blend: genetic basis and behavioural consequences

Evolutionary diversification of sexual communication systems in moths is perplexing because signal and response are under stabilizing selection in many species, and this is expected to constrain evolutionary change. In the moth Heliothis virescens, we consistently found high phenotypic variability in the female sex pheromone blend within each of four geographically distant populations. Here, we assess the heritability, genetic basis and behavioural consequences of this variation. Artificial selection with field-collected moths dramatically increased the relative amount of the saturated compound 16:Ald and decreased its unsaturated counterpart Z11–16:Ald, the major sex pheromone component (high line). In a cross between the high- and low-selected lines, one quantitative trait locus (QTL) explained 11–21% of the phenotypic variance in the 16:Ald/Z11–16:Ald ratio. Because changes in activity of desaturase enzymes could affect this ratio, we measured their expression levels in pheromone glands and mapped desaturase genes onto our linkage map. A delta-11-desaturase had lower expression in females producing less Z11–16:Ald; however, this gene mapped to a different chromosome than the QTL. A model in which the QTL is a trans-acting repressor of delta-11 desaturase expression explains many features of the data. Selection favouring heterozygotes which produce more unsaturated components could maintain a polymorphism at this locus.     

A quantitative genetic analysis of nuclear-cytoplasmic male sterility in structured populations of Silene vulgaris

Gynodioecy, the coexistence of functionally female and hermaphroditic morphs within plant populations, often has a complicated genetic basis involving several cytoplasmic male-sterility factors and nuclear restorers. This complexity has made it difficult to study the genetics and evolution of gynodioecy in natural populations. We use a quantitative genetic analysis of crosses within and among populations of Silene vulgaris to partition genetic variance for sex expression into nuclear and cytoplasmic components. We also use mitochondrial markers to determine whether cytoplasmic effects on sex expression can be traced to mitochondrial variance. Cytoplasmic variation and epistatic interactions between nuclear and cytoplasmic loci accounted for a significant portion of the variation in sex expression among the crosses. Source population also accounted for a significant portion of the sex ratio variation. Crosses among populations greatly enhanced the dam (cytoplasmic) effect, indicating that most among-population variance was at cytoplasmic loci. This is supported by the large among-population variance in the frequency of mitochondrial haplotypes, which also accounted for a significant portion of the sex ratio variance in our data. We discuss the similarities between the population structure we observed at loci that influence sex expression and previous work on putatively neutral loci, as well as the implications this has for what mechanisms may create and maintain population structure at loci that are influenced by natural selection.     

Juvenile sparrows preferentially eavesdrop on adult song interactions

Recent research has demonstrated that bird song learning is influenced by social factors, but so far has been unable to isolate the particular social variables central to the learning process. Here we test the hypothesis that eavesdropping on singing interactions of adults is a key social event in song learning by birds. In a field experiment, we compared the response of juvenile male song sparrows (Melospiza melodia) to simulated adult counter-singing versus simulated solo singing. We used radio telemetry to follow the movements of each focal bird and assess his response to each playback trial. Juveniles approached the playback speakers when exposed to simulated interactive singing of two song sparrows, but not when exposed to simulated solo singing of a single song sparrow, which in fact they treated similar to heterospecific singing. Although the young birds approached simulated counter-singing, neither did they approach closely, nor did they vocalize themselves, suggesting that the primary function of approach was to permit eavesdropping on these singing interactions. These results indicate that during the prime song-learning phase, juvenile song sparrows are attracted to singing interactions between adults but not to singing by a single bird and suggest that singing interactions may be particularly powerful song-tutoring events.     

Genetic prediction of complex traits: integrating infinitesimal and marked genetic effects

Genetic prediction for complex traits is usually based on models including individual (infinitesimal) or marker effects. Here, we concentrate on models including both the individual and the marker effects. In particular, we develop a “Mendelian segregation” model combining infinitesimal effects for base individuals and realized Mendelian sampling in descendants described by the available DNA data. The model is illustrated with an example and the analyses of a public simulated data file. Further, the potential contribution of such models is assessed by simulation. Accuracy, measured as the correlation between true (simulated) and predicted genetic values, was similar for all models compared under different genetic backgrounds. As expected, the segregation model is worthwhile when markers capture a low fraction of total genetic variance.     

Nestling sex ratios in a population of Bluethroats Luscinia svecica inferred from AFLP™ analysis

We studied the sex ratio of Bluethroat Luscinia svecica broods using AFLPs. Our aim was to test whether there is a bias towards males that could be explained by sexual selection theories, or conversely, a bias towards females that could help explain the female-biased sex ratio among juveniles observed at a wintering site. The AFLP technique was reliable in sexing the nestlings from even small initial DNA quantities. Given the large number of polymorphic markers that can be obtained for each primer combination, the probability of detecting a W-chromosome-linked fragment is reasonably high. As a consequence, this method could be used in other species for sex-ratio studies and for other genetic purposes. Among 246 nestlings, we found an overall proportion of males of 50.8% at hatching and the sex-ratio variation using broods as independent units was not significantly different from expectation under a binomial distribution. None of the parental and environmental variables tested changed significantly the deviance to the model. Thus, sex determination in the Bluethroat seems to match the classical Mendelian model of a 1:1 sex ratio and cannot explain the biased sex ratio towards juvenile females found at the wintering site.     

A microsatellite‐based linkage map for song sparrows (Melospiza melodia)

Although linkage maps are important tools in evolutionary biology, their availability for wild populations is limited. The population of song sparrows (Melospiza melodia) on Mandarte Island, Canada, is among the more intensively studied wild animal populations. Its long‐term pedigree data, together with extensive genetic sampling, have allowed the study of a range of questions in evolutionary biology and ecology. However, the availability of genetic markers has been limited. We here describe 191 new microsatellite loci, including 160 high‐quality polymorphic autosomal, 7 Z‐linked and 1 W‐linked markers. We used these markers to construct a linkage map for song sparrows with a total sex‐averaged map length of 1731 cM and covering 35 linkage groups, and hence, these markers cover most of the 38–40 chromosomes. Female and male map lengths did not differ significantly. We then bioinformatically mapped these loci to the zebra finch (Taeniopygia guttata) genome and found that linkage groups were conserved between song sparrows and zebra finches. Compared to the zebra finch, marker order within small linkage groups was well conserved, whereas the larger linkage groups showed some intrachromosomal rearrangements. Finally, we show that as expected, recombination frequency between linked loci explained the majority of variation in gametic phase disequilibrium. Yet, there was substantial overlap in gametic phase disequilibrium between pairs of linked and unlinked loci. Given that the microsatellites described here lie on 35 of the 38–40 chromosomes, these markers will be useful for studies in this species, as well as for comparative genomics studies with other species.     

Cultural and genetic evolution in mountain white-crowned sparrows: song dialects are associated with population structure

Bird song often varies geographically within a species; when this geographic variation has distinct boundaries, the shared song types are referred to as song dialects. How dialects are produced and their adaptive significance are longstanding problems in biology, with implications for the role of culture in the evolution and ecology of diverse organisms, including humans. Here we test the hypothesis that song dialect, a culturally transmitted trait, is related to the population genetic structure of mountain white-crowned sparrows (Zonotrichia leucophrys oriantha). To address this, we compared microsatellite allele frequencies from 18 sample sites representing eight dialect regions in the Sierra Nevada. Pairwise genetic distances were not significantly correlated with geographic distances either within or between dialects, nor did dialect groups form distinct genetic groups according to neighbor-joining or UPGMA analysis, and most variation in allele frequencies occurred among individuals rather than at higher levels. However, most of the remaining variation was attributable to differences among, rather than within, dialect regions, and this among-dialect component of variance was statistically significant. Moreover, when controlling for the effect of geographic distance, song dissimilarity and genetic distance between site pairs were significantly correlated. Thus, song dialects appear to be associated with reductions in, but not strict barriers to, gene flow among dialect regions.     

No evidence for inbreeding avoidance in a natural population of song sparrows (Melospiza melodia)

We studied mate choice and inbreeding avoidance a natural population of song sparrows (Melospiza melodia) on Mandarte Island, Canada. Inbreeding occurred regularly: 59% all matings were between known relatives. We tested for inbreeding avoidance by comparing the observed levels of inbreeding to those expected if mate choice had been random with respect to relatedness. Independent of our assumptions about the availability of mates in the random mating model, we found that the expected and observed distributions of inbreeding coefficients were similar, as was the expected and observed frequency of close (f >/= 0.125) inbreeding. Furthermore, there was no difference in relatedness observed pairs and those that would have resulted had birds mated instead with their nearest neighbors. The only evidence to suggest any inbreeding avoidance was a reduced rate of parent-offspring matings as compared to one random mating model but not the other. Hence, despite substantial inbreeding depression in this population, we found little evidence for inbreeding avoidance through mate choice. We present a simple model to suggest that variation in inbreeding avoidance behaviors in birds may arise from differences in survival rates: in species with low survival rates, the costs of forfeiting matings to avoid inbreeding may exceed the costs of inbreeding.     

On the evolutionary stability of Mendelian segregation

We present a model of a primary locus subject to viability selection and an unlinked locus that causes sex-specific modification of the segregation ratio at the primary locus. If there is a balanced polymorphism at the primary locus, a population undergoing Mendelian segregation can be invaded by modifier alleles that cause sex-specific biases in the segregation ratio. Even though this effect is particularly strong if reciprocal heterozygotes at the primary locus have distinct viabilities, as might occur with genomic imprinting, it also applies if reciprocal heterozygotes have equal viabilities. The expected outcome of the evolution of sex-specific segregation distorters is all-and-none segregation schemes in which one allele at the primary locus undergoes complete drive in spermatogenesis and the other allele undergoes complete drive in oogenesis. All-and-none segregation results in a population in which all individuals are maximally fit heterozygotes. Unlinked modifiers that alter the segregation ratio are unable to invade such a population. These results raise questions about the reasons for the ubiquity of Mendelian segregation.     

Effect of balancing selection on spatial genetic structure within populations: theoretical investigations on the self-incompatibility locus and empirical studies in Arabidopsis halleri

The effect of selection on patterns of genetic structure within and between populations may be studied by contrasting observed patterns at the genes targeted by selection with those of unlinked neutral marker loci. Local directional selection on target genes will produce stronger population genetic structure than at neutral loci, whereas the reverse is expected for balancing selection. However, theoretical predictions on the intensity of this signal under precise models of balancing selection are still lacking. Using negative frequency-dependent selection acting on self-incompatibility systems in plants as a model of balancing selection, we investigated the effect of such selection on patterns of spatial genetic structure within a continuous population. Using numerical simulations, we tested the effect of the type of self-incompatibility system, the number of alleles at the self-incompatibility locus and the dominance interactions among them, the extent of gene dispersal, and the immigration rate on spatial genetic structure at the selected locus and at unlinked neutral loci. We confirm that frequency-dependent selection is expected to reduce the extent of spatial genetic structure as compared to neutral loci, particularly in situations with low number of alleles at the self-incompatibility locus, high frequency of codominant interactions among alleles, restricted gene dispersal and restricted immigration from outside populations. Hence the signature of selection on spatial genetic structure is expected to vary across species and populations, and we show that empirical data from the literature as well as data reported here on three natural populations of the herb Arabidopsis halleri confirm these theoretical results.     

Hearing in the swamp sparrow,Melospiza georgiana,and the song sparrow,Melospiza melodia

Operant conditioning techniques and a psychophysical tracking procedure were used to measure thresholds for pure tones in two congeneric species of sparrows: swamp sparrows and song sparrows. Thresholds were measured both in quiet conditions and in the presence of white noise. The two species were similar in their gross pattern of auditory sensitivity with most sensitive thresholds in the frequency region of 1·0–8·0 kHz and poor hearing above and below this range. However, the best sensitivity occurred at 2 kHz for the song sparrows and at 4 kHz for the swamp sparrows. This pattern was also observed in song spectra of the two species. The songs of song sparrows had more power in lower frequencies than the songs of swamp sparrows. Masked auditory thresholds for both species were very similar, showing a generally increasing signal-to-noise ratio with increasing frequency. The similarity between swamp and song sparrows in these measures of basic auditory sensitivity suggests that the primary mechanisms underlying selective vocal learning in these sparrows probably reside at higher levels than the peripheral auditory sensitivities.