Genetic effects on sperm design in the zebra finch

Abstract

Sperm design and function are important determinants of male reproductive success and are expected to be under strong selection. The way that spermatozoa phenotypes evolve is poorly understood, because there have been few studies of the quantitative genetics of sperm. Here we show, in the zebra finch Taeniopygia guttata, an extraordinary degree of inter-male variation in sperm design that is independent of sperm swimming velocity. A quantitative genetics study using data from over 900 zebra finches in a complex breeding experiment showed that sperm head, mid-piece and flagellum length are heritable, that negative genetic correlations exist between sperm traits, and that significant indirect (maternal) genetic effects exist. Selection on the zebra finch sperm phenotype may be low because sperm competition is infrequent in this species, and this, in combination with negative genetic correlations and maternal genetic effects, may account for the variation in sperm phenotype between males. These results have important implications for the evolution of sperm in other taxa.

Patterns of genetic variation and covariation in ejaculate traits reveal potential evolutionary constraints in guppies

“…Indeed, midpiece length was not significantly genetically correlated with flagellum length, although the sign of both phenotypic and genetic correlations is consistent with previous work, revealing a negative correlations between midpiece length and flagellum length, both in guppies (phenotypic correlation; Skinner and Watt, 2007) and zebra finches (genetic correlation; Birkhead et al, 2005). In the zebra finch example, however, flagellum length is more closely associated with total sperm length than midpiece size, and therefore the strong positive genetic correlation between flagellum length and sperm swimming velocity will likely favour longer, not shorter, sperm in this species (Mossman et al, 2009).…”

“…Although an increasing (but still small) body of literature suggests that individual ejaculate traits can exhibit very high levels of additive genetic variation (reviewed by Simmons and Moore, 2009), there is also accumulating evidence that trade-offs between various ejaculate traits may constrain their evolvability. For example, in the cockroach, Nauphoeta cinerea, sperm viability is negatively genetically correlated with both testes mass and sperm numbers (Moore et al, 2004), whereas in the zebra finch, Taeniopygia guttata, midpiece size is negatively genetically correlated with the length of the sperm's head and flagellum (Birkhead et al, 2005). Both studies therefore highlight the potential for trade-offs to impede evolutionary responses to selection on individual ejaculate traits.…”

“…Thus, genetic approaches for studying sperm evolution are essential, and especially those that focus on multiple traits in order to shed light on their patterns of genetic covariance, and therefore the potential for genetic correlations to either facilitate or impede multivariate selection on ejaculate traits (for example, Simmons and Kotiaho, 2002;Moore et al, 2004;Birkhead et al, 2005;Snook et al, 2010). Although an increasing (but still small) body of literature suggests that individual ejaculate traits can exhibit very high levels of additive genetic variation (reviewed by Simmons and Moore, 2009), there is also accumulating evidence that trade-offs between various ejaculate traits may constrain their evolvability.…”

Inbreeding depression of sperm traits in the zebra finch Taeniopygia guttata

“…Indeed, comparative studies across songbirds have indicated that within‐ and between‐male variance in sperm length is removed through postcopulatory stabilizing selection acting against extreme sperm length (Birkhead et al. 2005; Calhim et al. 2007; Immler et al.…”

High morphological variation of vestibular system accompanies slow and infrequent locomotion in three-toed sloths

“…Links between reduced function, relaxed natural selection and greater variation has been acknowledged by more recent studies [19] and demonstrated to characterize certain vestigial traits of insects [20]. More distantly related but still relevant examples of reduced selection and increased variation include certain birds and fishes, which show greater sperm morphological variation coincident with a release of sexual selection [21,22]. In addition, reduced competition in Garter snakes may have increased variation heritability of colour patterns [23].…”