Heritability and genetic correlation between the sexes in a songbird sexual ornament

heritability estimates assuming complete Z-linked inheritance; coef. denote coefficients applied to the familial regressions and analysis of variances (ANOVAs) when assuming complete Z-linked inheri- tance; h² is not given for the mother–daughter regression as is predicted to be 0. N is the number of families used in each analysis.

Z-linked inheritance and maternal effect

The high heritabilities with both male grandparents and, in particular, the fact that the maternal half-sib estimate

greatly exceeds the theoretical maximum for heritability

(Table 1) gives support to the hypothesis that genes influencing FP size may not be situated on the autosomes

but, rather, on the sex chromosomes (Houde, 1992; Roff,

1997). Under Z-linkage, the coefficient of coancestry for

z
full-brothers becomes 3/4, and that between mothers and daughters should be 0 (see column h² in Table 1;

Trivers, 1985; Lynch and Walsh, 1997). Assuming complete Z-linked inheritance, the maternal grand-

father–grandson estimate takes a value similar to those based on parent–offspring comparisons (Table 1). How-

ever, the resemblance among maternal half-brothers remained very high (Table 1). This suggests that some

of our heritability estimates may be inflated by some type of maternal effect.

There was a positive relationship between the mothers condition while rearing nestlings and size of the

ornament her young of both sexes developed at adult- hood, after accounting for maternal and paternal genetic

influence (Table 2). Further, maternal condition inter- acted with the size of the male parent ornament, so that

individuals grew larger FPs in adulthood when they were sired by fathers bearing large ornaments and

mothers in prime condition (Table 2). In addition, there was a significant influence of hatching date on ornament

size that was dependent on individual’s sex. Females born late in the season grew larger FPs than females born

early in the season, while in males FP size did not vary in relation to hatching phenology (Table 2).

Table 2 Results of the GLIMMIX model explaining variation in standardised forehead patch (FP) size as a function of individual sex, birth date and paternal and maternal FP size and condition

w hile individuals were being cared for by their parents

age-dependent expression in female pied flycatchers

(Potti, 1993; J Potti and D Canal, paper under review)

Sex 1, 60 —0.06 (0.24) 0.06 0.8016

Hatching date 1, 60 0.83 (0.32) 6.19 0.0157
Sex x hatching date

Female 1, 60 0.79 (0.35) 5.12 0.0272

Male 0 — — — Size of father ’s FP 1, 60 0.43 (0.10) 17.91 0.0000

Size of mother ’s FP 1, 60 0.30 (0.11) 8.02 0.0063

Mother condition 1, 60 0.23 (0.12) 3.89 0.0531^a

have been able to suggest for the first time a significant genetic component to threshold sex trait expression in female vertebrates. Our testing of predictions of Z-linked vs autosomal inheritance stemming from Sætre et al. (2003) work gave evidence in support of both models, while discarding independent genetic control of trait size in males and females as recently suggested for the dung beetle Onthophagus sagittarius (Watson and Simmons,

2010). Below we discuss supporting evidence for auto- somal and Z-linked inheritance of FP size and its

^{Size of father ’s FP x}

mother condition

^{1, 60 0.23 (0.09) 5.84 0.0187}

expression in female pied flycatchers.

Before discussing the implications of our findings, we

Only significant explanatory fixed factors and covariates and/or

involved in significant interactions in the final model are shown. ^aEstimate (s.e.) for mother ’s condition after removing the father ’s FP x mother condition interaction term ¼ 0.25 (0.12), F ¼ 4.23, 61 d.f., P ¼ 0.0442.

Between-sex genetic correlation in ornament size

The phenotypic between-sex correlation (r_p) in FP size estimated from the female–male, full-sib comparison was r_p (s.e.) ¼ 0.41. (0.030); N ¼ 28, Po0.03. The estimate for the genetic correlation is r_MF ¼ 0.87 (s.e. 0.24), which does not differ significantly from r_G ¼ 1 (t ¼ —0.54, P40.50) while differing significantly from zero (t ¼ 3.62, Po0.001). This points out to a common genetic basis for the trait in both sexes, leaving little scope for the independent evolution of ornament size in each sex.
Discussion

We have shown that a secondary sex trait differentially expressed by all males and over one-third of females in a southern European population of pied flycatchers has a genetic basis common to both sexes. Males resembled both their male and female parents in the standardised size of their ornament, while females only resembled significantly to their fathers. To the best of our knowl- edge, this is one of the few studies measuring the phenotype of a secondary sexual trait in both parents and progeny as breeding adults and suggesting its genetic transmission through both germ lines in wild populations (review in Poissant et al., 2009). Previously, Roulin et al. (2001 and Roulin and Dijkstra, 2003) capitalised on the fact that both sexes express plumage

‘quality’ signals at the late nestling stage in barn owls to show that those traits also were genetically correlated between the sexes. As ours, their results implied that selection on one sex for a trait value would indirectly impose selection toward similar values in the other sex and that genes for sex-specific traits can be expressed in the other one because of the between-sex genetic correlation (Lande, 1980, 1987). Although it may be argued that our long-term non-experimental approach could suffer from environmental causes of resemblance (cf. Roulin et al., 2001; Rowe and Day, 2006), our cross- fostering experiment unambiguously demonstrated a significant additive genetic component to the trait, at least in males. Limited expression of the ornament and

should briefly consider if extra-pair fertilisations, which being relatively frequent in pied flycatchers (Lifjeld et al.,

1991; Gelter and Tegelstro¨ m, 1992; Bru¨ n et al., 1996; Moreno et al., 2010), could be biasing our estimates of resemblance. Our data on extra pair fertilisations (D Canal, J Potti and JA Da^´ vila, paper under review) do not allow for a proper estimation of their effect on trait heritability because of a combination of two events with low frequency, that is, recruiting to adult age (which is needed for the ornament being measured; average recruitment rate ¼ 14%, both sexes combined; N ¼ 14 years and 4536 fledglings; Potti and Montalvo, 1991b, Lehtonen et al., 2009) and being sired by a male other than the social ‘father ’ (average rate of extra-pair paternity about 15%; D Canal and J Potti, unpublished data). However, as there is no intraspecific brood parasitism in our population, heritabilities calculated with mothers are less prone to this kind of bias than those made with fathers, when mistakenly taking the cuckolded males caring for young in a nest as the genetic father should decrease male–offspring resemblances (Charmantier and Re^´ ale, 2005). Further, ‘classical’ (that is, autosomal) heritabilities did not differ in relation to the sex of parents, suggesting that the unknown rate of misassigned paternity in our long-term database is not biasing the estimates of heritability. In this sense, the absence of differences between both grandparent–grand- offspring estimates of resemblance suggests that the effect of extra-pair paternity is not strong because, if it were, we should expect a lower resemblance for grand- offspring in the paternal line. Thus, we conclude that, irrespective of the mode of inheritance of ornament size, the heritabilities here presented are likely conservative estimates.

The forehead ornament of black-and-white, European Ficedula flycatchers has been proposed as being linked to the Z chromosome on the basis of evidence based on variation in single-nucleotide polymorphisms (Sætre et al., 2003), although the investigators were careful in recognising that other phenomena, such as the co-linearity they noted between the Z chromosome and autosomes, could have influenced the patterns they observed. Our evidence was mixed when patterns of inheritance (autosomal vs Z-linked) in ornament size were explored. On one hand, the FP size in females was nearly half the size, on average, of that of males. This is consistent with a model based on Z-linked additive genetic inheritance without dosage compensation in