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


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female endocrine environment (Gil et al., 2006).

The genetic correlation between the sexes was near

unity, indicating a strong constraint for the evolution of sexual dimorphism in FP size. This could be a case of an

initially ‘vestigial’ (Darwin, 1874; Lande, 1980; reviewed by Bonduriansky and Chenoveth, 2009) trait in females

being a product of a genetic correlation between the

sexes and favoured in males that has been functionally sequestered to also signal quality in females, thus

creating correlated selection between the sexes. The population may not be in equilibrium but rather in the

transitional stage envisaged in the models of Lande

(1980, 1987) of rapid, parallel evolution of male and

female characters, which hypothetically, would be followed by a phase of selection acting differentially on

each sex, with forces of nearly the same magnitude but of opposite sign. That stage seems not yet reached, maybe

because the high between-sex genetic correlation makes the evolution of sexual dimorphism an exceedingly slow

process (Lande, 1980, 1987; Bonduriansky and Rowe,

2005; Bonduriansky and Chenoveth, 2009; Poissant et al.,

2009). Once exposed to selection, however, all agents of natural and sexual selection on the ornament may not be


z
necessarily coincident in both sexes and/or, given the differences in additive genetic variance (Table 1; h2

values), would result in similar responses (Lynch and

Walsh, 1997; Badyaev, 2002). For instance, if the expres-

sion of the ornament in females (which they develop almost always when aged 2 years or older; Potti, 1993) is

dependent on hormonal control of gene expression while male displaying is more genetically determined—that is,

in the present context, decoupled from genetically programmed or environmentally induced hormonal or

genetic switch-offs, selection will act differently on both sexes, if only by being dependent on the interaction

between the genetic and environmental components of the hormonal responses across sexes (Dufty et al., 2002).

Thus, although female showiness could be explained

primarily with reference to selective processes directly

affecting females (Amundsen 2000) genetic constraints may also be paramount (Roulin and Dijkstra, 2003; this

study;reviewed by Poissant et al., 2009).

Our results put forward the intriguing problem if and

why, judging from the abundant literature on the genus, female expression of the ornament has been almost

altogether suppressed in most northern Eurasian black- and-white flycatcher (F. h. hypoleuca and F. albicollis)

populations, in contrast to Iberian (F. h. iberiae) ones

(Lundberg and Alatalo, 1992; Cramp and Perrins, 1993;

cf. Potti, 1993; Morales et al., 2007). Once that genetic and environmental contributions to ornament size in black-

and-white European Ficedula species are beginning to be

understood (Sheldon et al., 1997; Qvarnstro¨ m, 1999; Hegyi et al., 2002; Sætre et al., 2003; Sæther et al., 2007; this study), the biggest challenge is now for researchers to explain the within and between-population differ- ences in the degree of inhibition (Williams and Carroll,

2009) of ornament displaying in females, a trait that we show is apparently subject to large environmental/non- additive genetic variance(s). When optimal trait expres- sion differs between the sexes, between-sex population variation in its degree might cause geographically variable antagonistic selection (Mank et al., 2007), where- in genetic factors spread across populations by giving a reproductive advantage to males while disadvantaging females or vice versa. We need more phenotypic information from central and northern European loca- tions as it seems likely that geographic differences in the degree of expression of apparently sex-limited traits (note we do not necessarily imply sex-linked traits) may contribute significantly to phenotypic differences among populations (Poissant et al., 2009). Differences in both the expression and function of characters shared by males and females can tell us much on sex differences in life- history, mate preferences and degree of sexual antagon- ism within and across populations (Badyaev, 2002; Rowe and Day, 2006). Our knowledge of interactions between- sex chromosomes and autosomes contributing to sexual dimorphisms and antagonistic co-evolution in evolu- tionary important traits will be furthered on by devel- opment of genetic markers and genomic approaches (Wright et al., 2007) being subsequently related to sex and population variation in expression, size and function of those traits.


Conflict of interest

The authors declare no conflict of interest.


Acknowledgements
Over the years, JP’s work has been funded by the Spanish Ministries of Education, Science and Culture, most recently by projects CGL2006-07481/BOS and CGL2009-10652/BOS. DC was supported by a grant from the Ministerio de Educacio´ n y Ciencia (I3P- BDP2005). We are most grateful to Roger Jovani, David Serrano, Jose´ Luis Tella, Juan Jose´ Negro and La´ szlo´ Zsolt Garamszegi for valuable input, to Eloy Revilla and Ne´ stor Ferna´ ndez for guidance with bootstrapping and to AJ Moore for advice on an earlier draft of the paper. We also thank two reviewers for insightful comments.

References


Amundsen T (2000). Why are female birds ornamented? Trends

Ecol Evol 15: 149–155.

Badyaev AV (2002). Growing apart: an ontogenetic perspective

on the evolution of sexual size dimorphism. Trends Ecol Evol

17: 369–378.

Becker WA (1984). Manual of Quantitative Genetics. Academic

Enterprises: Pullman, Washington, DC.

Bonduriansky R, Rowe L (2005). Intralocus sexual conflict and

the genetic architecture of sexually dimorphic traits in

Prochyliza xanthostoma (Diptera: Piophilidae). Evolution 59:

1965–1975.

Bonduriansky R, Chenoweth SF (2009). Intralocus sexual

conflict. Trends Ecol Evol 24: 280–288.

Bru¨ n J, Winkel W, Epplen JT, Lubjuhn T (1996). Parentage analyses in the pied flycatcher (Ficedula hypoleuca) at the western boundary of its central European range. J Orn 137: 435–446.

Charlesworth B, Coyne JA, Barton N (1987). The relative rates of evolution of sex chromosomes and autosomes. Am Nat 130:

113–146.


Charmantier A, Re´ ale D (2005). How do misassigned paternities

affect the estimation of heritability in the wild? Mol Ecol 14:

2839–2850.

Cramp S, Perrins CM (1993). Handbook of the Birds of Europe, the

Middle East and North Africa Volume VII: Flycatchers to Shrikes. Oxford University Press: Oxford.

Darwin C (1874). Sexual Selection and the Descent of Man. Spanish translation, 1989.El origen del hombre y la seleccio´ n en

relacio´ n al sexo EDAF: Madrid.

Dufty Jr AM, Clobert J, MØller AP (2002). Hormones,

developmental plasticity and adaptation. Trends Ecol Evol

174: 190–196.

Ellegren H (2009). Genomic evidence for a large-Z effect. Proc R Soc Lond B 276: 361–366.

Ellegren H, Hultin-Rosenberg L, Brunstro¨ m B, Dencker L, Kultima K, Scholz B (2007). Faced with inequality: chicken do not have a general dosage compensation of sex-linked genes. BMC Biol 5: 40, http://www.biomedcentral.com/

1741-7007/5/40.

Fairbairn DJ, Roff DA (2006). The quantitative genetics of sexual

dimorphism: assessing the importance of sex-linkage.

Heredity 97: 319–328.

Falconer DS, MacKay TFC (1996). Introduction to Quantitative

Genetics. 4th edn. Longmann: London.

Fisher RA (1958). The Genetical Theory of Natural Selection. 2nd

edn. Dover: New York.

Fitzpatrick MJ (2004). Pleiotropy and the genomic location of sexually selected genes. Am Nat 163: 800–808.

Gelter HP, Tegelstro¨ m M (1992). High frequency of extra-pair paternity in Swedish Pied Flycatchers revealed by allozyme electrophoresis and DNA fingerprinting. Behav Ecol Sociobiol

31: 1–7.

Gil D, Lacroiz A, Potti J (2006). Within-clutch variation in yolk

androgens in relation to female expression of a male ornament in pied flycatchers (Ficedula hypoleuca). Ardeola 53:

307–315.


Griggio M, Devigili A, Hoi H, Pilastro A (2009). Female

ornamentation and directional male mate preference in the rock sparrow. Behav Ecol 20: 1072–1078.

Hegyi G, To¨ ro¨ k J, To´ th J (2002). Qualitative population divergence in proximate determination of a sexually selected

trait in the collared flycatcher. J Evol Biol 15: 710–719.

Houde AE (1992). Sex-linked heritability of a sexually selected

character in a natural population of Poediia reticulata (Pisces:

Poeciliidae) (guppies). Heredity 69: 229–235.

Itoh Y, Melamed E, Yang X, Kampf K, Wang S, Yehy N et al.

(2007). Dosage compensation is less effective in birds than in mammals. J Biol 6: 2.

Iyengar VK, Reeve HK, Eisner T (2002). Paternal inheritance of

a female moth’s mating preference. Nature 419: 830–832.

Kimball RT, Ligon JD (1999). Evolution of avian plumage

dichromatism from a proximate perspective. Am Nat 154:

182–193.


Kirkpatrick M, Hall DW (2004). Male-biased mutation, sex

linkage, and the rate of adaptive evolution. Evolution 57: 437–440. Kirkpatrick M, Ryan MJ (1991). The evolution of mating

preferences and the paradox of the lek. Nature 350: 33–38. Lande R (1980). Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34: 292–305. Lande R (1987). Genetic correlations between the sexes in the

evolution of sexual dimorphism and mating preferences. In: Bradbury JW, Andersson MB (eds). Sexual Selection: Testing the Alternatives,. John Wiley and Sons: Dahlem, 83–94.

Lehtonen PK, Laaksonen T, Artemyev AV, Belskii E, Both C, Buresˇ S et al. (2009). Geographic patterns of genetic differenti-

ation and plumage colour variation are different in the pied flycatcher (Ficedula hypoleuca). Mol Ecol 18: 4463–4476.

Lifjeld JT, Slagsvold T, Lampe HM (1991). Low frequency of

extrapair paternity in pied flycatcher revealed by DNA

fingerprinting. Behav Ecol Sociobiol 29: 95–101.

Lundberg A, Alatalo RV (1992). The Pied Flycatcher. Poyser: London. Lynch M, Walsh B (1997). Genetics and Analysis of Quantitative

Traits. Sinauer: Sunderland, MA.

Mank JE, Axelsson E, Ellegren H (2007). Fast-X on the Z:

rapid evolution of sex-linked genes in birds. Genome Res 17:

618–624.


Mank JE, Ellegren H (2007). Parallel divergence and degradation

of the avian W sex chromosome. Trends Ecol Evol 22: 389–391. Mank JE, Ellegren H (2009). Sex-linkage of sexually antagonistic genes is predicted by female, but not male, effects in birds.

Evolution 63: 1464–1472.

Mank JE, Hall DW, Kirkpatrick M, Avise JC (2006). Sex

chromosomes and male ornaments: a comparative evalua- tion in ray-finned fishes. Proc R Soc Lond B 273: 233–236.

Mank JE, Hultin-Rosenberg L, Zwahlen M, Ellegren H (2008).

Pleiotropic constraint hampers the resolution of sexual antagonism in vertebrate gene expression. Am Nat 171: 35–43. Mank JE, Vicoso B, Berlin S, Charlesworth B (2010). Effective population size and the faster-X effect: empirical results and

their interpretation. Evolution 64: 663.

McKenna NJ, O’Malley BW (2002). Combinatorial control of

gene expression by nuclear receptors and coregulators. Cell

108: 465–474.

Merila¨ J, Sheldon BC (2001). Avian quantitative genetics. In: Nolan V, Ketterson E (eds). Current Ornithology, Vol. 16

Kluwer Academic/Plenum Publishers: New York, 179–255.

Merila¨ J, Sheldon BC, Ellegren H (1998). Quantitative genetics of sexual size dimorphism in the collared flycatcher, Ficedula albicollis. Evolution 52: 870–876.

MØller AP (1993). Sexual selection in the barn swallow Hirundo rustica. III Female tail ornaments. Evolution 47: 417–431.

Moore AJ, Moore PJ (2006). Genetics of sexual selection. In: Fox

CW, Wolf JB (eds). Evolutionary Genetics Concepts and Case

Studies. Oxford University Press: New York, 339–349. Morales J, Moreno J, Merino S, Sanz JJ, Toma´ s G, Arriero E et al.

(2007). Female ornaments in the Pied Flycatcher Ficedula hypoleuca: associations with age, health and reproductive

success. Ibis 149: 245–254.

Moreno J, Mart´ınez JG, Morales J, Lobato E, Merino S, Toma´ s G

et al. (2010). Paternity loss in relation to male age, territorial behaviour and stress in the pied flycatcher. Ethology 116: 76–84.

Nagylaki T 1978. The correlation between relatives with

assortative mating. Ann Hum Genet 42: 131–137.

O’Neill M, Binder M, Smith C, Andrews J, Reed K, Smith M

et al. (2000). ASW: a gene with conserved avian W-linkage and female specific expression in chick embryonic gonad. Dev Genes Evol 210: 243–249.

Osorno JL, Morales J, Moreno J, Merino S, Toma´ s G, Va´ squez R

(2006). Evidence for differential maternal allocation to eggs in relation to manipulated male attractiveness in the Pied Flycatcher (Ficedula hypoleuca). J Ornithol 147: 605–611.

Poissant J, Wilson AJ, Coltman DW (2009). Sex-specific genetic

variance and the evolution of sexual size dimorphism: a systematic review of cross-sex genetic correlations. Evolution

64: 97–107.

Potti J (1993). A male trait expressed in female pied flycatchers,

Ficedula hypoleuca: the white forehead patch. Anim Behav 45:

1245–1247.

Potti J (1999). Maternal effects and the pervasive impact of nestling

history on egg size in a passerine bird. Evolution 53: 279–285. Potti J (2008). Temperature during egg formation and the effect

of climate warming on egg size in a small songbird. Acta

Oecol 33: 387–393.

Potti J, Blanco G, Lemus JA´ , Canal D (2007). Infectious offspring: how birds acquire and transmit an avian poly-

omavirus in the wild. PLoS ONE 2: e1276.

Potti J, Merino S (1994). Heritability estimates and maternal

effects on tarsus length in pied flycatchers, Ficedula hypoleuca.

Oecologia 100: 331–338.

Potti J, Merino S (1996a). Decreased levels of blood trypano-

some infection correlate with female expression of a male secondary sexual trait: implications for sexual selection. Proc R Soc Lond B 263: 1199–1204.

Potti J, Merino S (1996b). Parasites and the ontogeny of sexual size dimorphism in a passerine bird. Proc R Soc Lond B 263: 9–12.

Potti J, Montalvo S (1991a). Male arrival and female mate choice

in pied flycatchers Ficedula hypoleuca in central Spain. Ornis

Scand 22: 45–54.

Potti J, Montalvo S (1991b). Return rate, age at first breeding

and natal dispersal of Pied Flycatchers Ficedula hypoleuca in central Spain. Ardea 79: 419–428.

Price DK (1996). Sexual selection, selection load and quantita-

tive genetics of zebra finch bill colour. Proc R Soc Lond B 263:

217–221.

Price DK, Burley NT (1993). Constraints on the evolution of

attractive traits: genetic (co)variance of zebra finch bill colour.

Heredity 71: 405–412.

Price DK, Burley NT (1994). Constraints on the evolution of

attractive traits: selection in male and female zebra finches.

Am Nat 144: 908–934.

Qvarnstro¨ m A (1999). Genotype-by-environment interactions in the determination of the size of a secondary sexual character in the collared flycatcher (Ficedula albicollis). Evolution 53:

1564–1572.

Qvarnstro¨ m A, Bailey RI (2008). Speciation through evolution of sex-linked genes. Heredity 102: 4–15.

Qvarnstro¨ m A, Brommer JE, Gustafsson L (2006). Testing the genetics underlying the co-evolution of mate choice and ornament in the wild. Nature 441: 84–86.

R Development Core Team (2005). R: A Language and Environ-

ment for Statistical Computing, Reference Index. R Foundation for Statistical Computing: Vienna. ISBN 3-900051-07-0, URL:http://www.R-project.org.

Reinhold K (1998). Sex linkage among genes controlling sexually selected traits. Behav Ecol Sociobiol 44: 1–7.

Rice WR (1984). Sex-chromosomes and the evolution of sexual

dimorphism. Evolution 38: 735–742.

Rice WR (1988). The effect of sex chromosomes on the rate of

evolution. Trends Ecol Evol 3: 2–3.

Roff DA (1997). Evolutionary Quantitative Genetics. Chapman

and Hall: New York.

Roulin A, Dijkstra C (2003). Genetic and environmental

components of variation in eumelanin and phaeomelanin sex traits in the barn owl. Heredity 90: 359–364.

Roulin A, Dijkstra C, Riols C, Ducrest A-L (2001). Female- and

male-specific signals of quality in the barn owl. J Evol Biol 14:

255–266.

Rowe L, Day T (2006). Detecting sexual conflict and sexually

antagonistic coevolution. Phil Trans R Soc B 361: 277–285. Rowe L, Houle D (1996). The lek paradox and the capture of

genetic variance by condition dependent traits. Proc R Soc

Lond B 263: 1415–1421.

Sætre G-P, Borge T, Lindross K, Haavie J, Sheldon BC, Primmer

C et al. (2003). Sex chromosome evolution and speciation in

Ficedula flycatchers. Proc R Soc Lond B 270: 53–59.

Sæther SA, Sætre GP, Borge T, Wiley C, Svedin N, Andersson G et al. (2007). Sex chromosome–linked species recognition and evolution of reproductive isolation in flycatchers. Science 318:

95–97.


SAS Institute Inc (2004). SAS/STATs 9.1. User’s Guide. SAS Institute Inc.: Cary.

Sheldon BC, Merila¨ J, Qvarnstro¨ m A, Gustafsson L, Ellegren H (1997). Paternal genetic contribution to offspring condition predicted by size of male secondary sexual character. Proc R Soc Lond B 264: 297–302.

Statsoft Inc (1996). Statistica for Windows, Release 5. Computer

Program Manual: Tulsa, OK.

Storchova´ R, Reif J, Nachman MW (2009). Female heterogamety and speciation: reduced introgression of the

Z chromosome between two species of nightingales.

Evolution 64: 456–471.

Trivers R (1985). Social Evolution. Benjamin/Cummings Publ

Co: Menlo Park, CA.

Ward PI (2000). Sperm length is heritable and sex-linked in the yellow dung fly (Scathophaga stercoraria). J Zool Lond 251:

349–353.

Watson NL, Simmons LW (2010). Male and female secondary sexual traits show different patterns of quantitative genetic and environmental variation in the horned beetle Onthophagus sagittarius. J Evol Biol 23: 2397–2402.



Williams TM, Carroll SB (2009). Genetic and molecular insights into the development and evolution of sexual dimorphism. Nature Rev 10: 797–804.

Wright D, Kerge S, Bra¨ ndstro¨ m H, Schu¨ tz K, Kindmark A, Andersson L et al. (2007). The genetic architecture of a female sexual ornament. Evolution 62: 86–98.
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