American Society of Naturalists

A membership society whose goal is to advance and to diffuse knowledge of organic evolution and other broad biological principles so as to enhance the conceptual unification of the biological sciences.

“Proximate causes of infertility and embryo mortality in captive zebra finches”

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Yifan Pei, Wolfgang Forstmeier, Daiping Wang, Katrin Martin, Joanna Rutkowska, and Bart Kempenaers (Nov 2020)

High rates of infertility and embryo mortality in zebra finches are puzzling but partly explained by sexual antagonism

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A family of zebra finches (<i>Taeniopygia guttata</i>). The mother (left) is feeding one of the three fledglings while the father (right) is watching the surrounding.<br/>(Drawing by Yifan Pei)
A family of zebra finches (Taeniopygia guttata). The mother (left) is feeding one of the three fledglings while the father (right) is watching the surrounding.
(Drawing by Yifan Pei)

In a wide range of species, including humans and birds, some couples experience difficulties with reproduction. Are such problems mostly a matter of age, of inbreeding (the pairing of close relatives), or of poor early-life conditions? Is reproductive failure caused by the male, the female, or by the specific combination of both partners? Are reproductive problems encoded in the genes, and if so, why do such detrimental genes exist in the first place? Scientists and the general public alike have long been puzzled by the causes of infertility and embryo mortality. However, thorough quantitative analyses of reproductive failure are rare, even in relatively well-studied species.

To answer those questions, researchers from the Max Planck Institute for Ornithology in Germany monitored and studied the fate of more than twenty-three thousand eggs in a captive population of zebra finches. They found that infertility is predominantly a male-specific problem, whereas embryo and nestling mortality are mostly a matter of the female. However, the main causes of infertility and offspring mortality remain unidentified. Age, inbreeding, and early-life conditions all have significant effects on reproductive performance, but explain only a little of the observed individual differences. This study provides further insights into the genetic causes of reproductive failure. Using quantitative genetic analysis, the researchers found that some of the genetic variants underlying male infertility tend to have beneficial effects on females, which might explain why such genetic variants can persist in the population.


Abstract

Some species show high rates of reproductive failure, which is puzzling because natural selection works against such failure in every generation. Hatching failure is common in both captive and wild zebra finches (Taeniopygia guttata), yet little is known about its proximate causes. Here we analyze data on reproductive performance (fate of >23,000 eggs) based on up to 14 years of breeding of four captive zebra finch populations. We find that virtually all aspects of reproductive performance are negatively affected by inbreeding (mean r = −0.117), by an early-starting, age-related decline (mean r = −0.132), and by poor early-life nutrition (mean r = −0.058). However, these effects together explain only about 3% of the variance in infertility, offspring mortality, fecundity and fitness. In contrast, individual repeatability of different fitness components varied between 15% and 50%. As expected, we found relatively low heritability in fitness components (median: 7% of phenotypic, and 29% of individually repeatable variation). Yet, some of the heritable variation in fitness appears to be maintained by antagonistic pleiotropy (negative genetic correlations) between male fitness traits and female and offspring fitness traits. The large amount of unexplained variation suggests a potentially important role of local dominance and epistasis, including the possibility of segregating genetic incompatibilities.