A novel test of the phenotype–linked fertility hypothesis reveals independent components of fertility

Abstract

The phenotype-linked fertility hypothesis predicts that male sexual ornaments signal fertilizing efficiency and that the coevolution of male ornaments and female preference for such ornaments is driven by female pursuit of fertility benefits. In addition, directional testicular asymmetry frequently observed in birds has been suggested to reflect fertilizing efficiency and to covary with ornament expression. However, the idea of a phenotypic relationship between male ornaments and fertilizing efficiency is often tested in populations where environmental effects mask the underlying genetic associations between ornaments and fertilizing efficiency implied by this idea. Here, we adopt a novel design, which increases genetic diversity through the crossing of two divergent populations while controlling for environmental effects, to test: (i) the phenotypic relationship between male ornaments and both, gonadal (testicular mass) and gametic (sperm quality) components of fertilizing efficiency; and (ii) the extent to which these components are phenotypically integrated in the fowl, Gallus gallus. We show that consistent with theory, the testosterone-dependent expression of a male ornament, the comb, predicted testicular mass. However, despite their functional inter-dependence, testicular mass and sperm quality were not phenotypically integrated. Consistent with this result, males of one parental population invested more in testicular and comb mass, whereas males of the other parental population had higher sperm quality. We found no evidence that directional testicular asymmetry covaried with ornament expression. These results shed new light on the evolutionary relationship between male fertilizing efficiency and ornaments. Although testosterone-dependent ornaments may covary with testicular mass and thus reflect sperm production rate, the lack of phenotypic integration between gonadal and gametic traits reveals that the expression of an ornament is unlikely to reflect the overall fertilizing efficiency of a male.

Testicular Growth and Comb and Wattles Development in Three Italian Chicken Genotypes Reared Under Free-Range Conditions

“…A positive relationship between comb size and sperm quality seemed to be strain specific (Gebriel et al, 2009;El Ghany et al, 2011;Udeh et al, 2011). Some studies reported no relationship between comb size and sperm quality (Pizzari et al, 2004;Bilcik and Estevez, 2005;Baczynski, 2008;Prieto et al, 2011), while others reported a negative relationship between comb size and sperm movement (Parker et al, 2006;Navara et al, 2012).…”

Sperm morphology, swimming velocity, and longevity in the house sparrow Passer domesticus

“…We also recorded the number of sperm cells detected by the CASA plug-in because moving sperm are likely to interfere more with each other at higher densities, a parameter we could not control. Sperm velocity has previously been described using VSL, VAP, or VCL or a combination of these parameters (Holt et al 1997;Froman and Feltmann 2000;Gage et al 2004;Pizzari et al 2004). In our samples, these parameters were strongly correlated with each other (r, 0.93-0.998; all P<0.0001).…”

Quantity matters: male sex pheromone signals mate quality in the parasitic wasp Nasonia vitripennis

“…Birkhead & Fletcher 1995;Parker et al 2006). Furthermore, these traits do not inevitably translate into an increased fertilizing efficiency (Pizzari et al 2004;Pilastro et al 2008); thus, actual fecundity benefits for the selective females have only rarely been demonstrated (Wagner & Harper 2003;Malo et al 2005a,b;Rogers et al 2008).…”