Summary
Life history theory predicts that individuals paired with attractive mates may invest more in offspring. Such differential investment may amplify the effects of genetic quality on fitness. Attractiveness can include ‘good gene’ and ‘complementary gene’ components, but how the latter affects parental investment remains unknown. We found that nestling song sparrows with genetically dissimilar parents grew faster than did nestlings whose parents were genetically more similar to one another. A cross-fostering experiment revealed complementary gene effects on growth; nestlings produced by genetically dissimilar parents grew faster than their adoptive ‘siblings’ reared in the same nest but produced by parents that were more genetically similar. To explore whether parental investment exaggerates these complementary gene effects on growth, we monitored parental nest visits. Maternal visits were negatively related to genetic similarity between mates. The novel finding that females adjust levels of care according to the genetic diversity of their offspring suggests that parental investment can amplify complementary gene effects on fitness.
Methodology
Study Population and General Field Techniques
We studied genetic similarity between mated pairs, nestling growth rates and parental care in eastern song sparrows (M. m. melodia) breeding near Newboro, Ontario, Canada (44°38′ 60N, 76°19′ 0W) in 2007 and 2008. In this population, socially mated pairs vary substantially in the degree to which they are genetically similar, as assessed by microsatellite profiles. We captured breeding adults in mist nets or seed-baited treadle traps in April 2007 and 2008, before the onset of nesting, and outfitted each with a unique combination of coloured leg bands. We collected a small blood sample (<25 μl) from each adult via brachial venipuncture, for genetic analysis.
In this and other populations of song sparrows, male song complexity is correlated with body condition (Pfaff et al. 2007), immunocompetence (Reid et al. 2005a) and fledging success (Reid et al. 2005b), any of which might confound our estimates of nestling growth rates and/or parental effort. To control for potential effects of song complexity, we determined the syllable repertoire size of territorial males. Following the criteria established by Pfaff et al. (2007) for this study population, we considered a male's repertoire to be recorded in full once 300 consecutive or 450 nonconsecutive songs had been recorded. We generated song spectrograms in Syrinx 2.6h (J. Burt; www.syrinxpc.com) and classified each male's complete set of recordings into distinct song and syllable types by visual analysis and sorting following MacDougall-Shackleton et al. (2009).
Genetic Similarity
To estimate genetic similarity between social mates, we genotyped all adults at seven hypervariable microsatellite loci: Mme 2 and Mme 7 (Jeffery et al. 2001); Escμ 1 (Hanotte et al. 1994); Pdoμ 5 (Griffith et al. 1999); SOSP 3, SOSP 13 and SOSP 14 (L. Keller, personal communication). One primer at each locus was dye-labelled and microsatellites were amplified using polymerase chain reaction (PCR). PCR was conducted in a total volume of 10 μl and included 10 mM of Tris-HCl, 50 mM of KCl, 0.1% Triton X-100, 0.2 mg/ml of BSA, 2.5 mM of MgCl2, 0.2 mM of each dNTP, 0.1–0.4 mM of each primer, 0.5 U Taq of polymerase (Fisher Scientific) and approximately 25 ng of genomic DNA. Cycling conditions included an initial step of 60 s at 94 °C, followed by 29 cycles of 30 s at 94 °C, 30 s at the annealing temperature (90 s for Sosp 3, 13 and 14), and 60 s at 72 °C, plus a final step of 270 s at 72 °C. Annealing temperatures were 54 °C for Pdoμ 5 and 57 °C for Sosp 3, 13 and 14. Escμ 1, Mme 2 and Mme 7 were amplified in a touchdown reaction with annealing temperatures dropping from 58 °C to 53 °C.
The resultant PCR products were analysed on a Beckman-Coulter CEQ 8000 or an Applied Biosystems 3130 Genetic Analyzer according to the manufacturers' protocols. We tested for deviations from Hardy–Weinberg expectations and from linkage equilibrium using GENEPOP version 3.3 (Raymond & Rousset 1995) and found no evidence for either. We calculated Wang's (2002) coefficient of genetic similarity, r, between each pair of social mates using the program MARK (K. Ritland, http://genetics.forestry.ubc.ca/ritland/programs.html).