In the Gouldian finch, captive females paired with genetically incompatible (different head-colour morph) males were shown in a 2010 Science study to bias paternity strongly toward compatible extra-pair males after a single controlled extra-pair copulation — a 'genetically loaded' process of sperm competition proposed as an adaptive function of female infidelity in socially monogamous animals. The causal process producing this bias was never identified, and the phenomenon's subsequent history is contested: the only wild-population study found no trace of the effect, and the domesticated stock used in the original experiments is known to be genetically divergent from wild birds. The open problem is: causally partition the compatibility-biased fertilization among cryptic female choice, strategic male sperm allocation, differential sperm viability, and ejaculate × female-tract interactions, and establish whether the process operates at measurable strength in natural populations. Cross-taxon generality — whether analogous postcopulatory targeting of compatible genes exists in other taxa — is retained as related background rather than a required component.

Background

In most bird species a male and female raise young together (social monogamy), yet individuals of both sexes commonly copulate outside the pair bond. Such matings are called extra-pair copulations (EPCs), and the offspring they sire, detected by molecular paternity analysis, constitute extra-pair paternity (EPP). Because a male's fitness rises directly with the number of females he fertilizes, the adaptive value of EPCs for females has been a long-standing controversy in evolutionary ecology. One class of proposed benefits is genetic: by mating with several males, a female could allow competition among their ejaculates inside her reproductive tract — sperm competition — and thereby be fertilized by the male whose genes are most compatible with her own, for example avoiding the elevated offspring mortality that follows when incompatible genomes are combined. If the female's own physiology biases which male's sperm is used, this is cryptic female choice; classic criteria (Birkhead 1998) demand that any such claim first exclude male-side alternatives, notably strategic adjustment by males of ejaculate size or sperm number, and sperm-intrinsic differences in viability or performance.

The Gouldian finch (Erythrura gouldiae) of northern Australia is a textbook system for genetic incompatibility. Head colour is a discrete polymorphism, red or black, controlled by a sex-linked locus on the Z chromosome (birds have ZW sex chromosomes, so males carry two Z chromosomes and females one Z and one W) — since mapped to a roughly 70-kilobase non-coding region near the follistatin (FST) gene. Red is dominant, so red-phenotype birds include both homozygotes and heterozygotes, which cannot be told apart by eye. Pairings between the two morphs suffer postzygotic genetic incompatibility: markedly higher embryo and nestling mortality, falling disproportionately on daughters (Pryke & Griffith 2009, Evolution). Female Gouldian finches constrained to pair with an incompatible, different-morph male respond with a suite of adjustments documented in companion studies: reduced maternal investment and broods overproducing sons, the sex less affected by incompatibility (Pryke & Griffith 2009, Science), together with chronically elevated corticosterone, a stress hormone (Griffith, Pryke & Buttemer 2011).

In the 2010 Science paper, Pryke, Rollins and Griffith gave captive, experimentally paired females one controlled EPC and genotyped the resulting offspring. The paternity outcome was strongly 'genetically loaded'. When the extra-pair male was compatible and the social male incompatible (an 'adaptive' context), the extra-pair male sired 76.5% of offspring from eggs fertilizable after the EPC, although he accounted for only about 6% of the female's copulations; in neutral contexts (both males of equal compatibility) a single EPC still yielded roughly 27–29% of offspring; and in the 'maladaptive' context, where the extra-pair male was the incompatible one, paternity was biased away from him. Extra-pair fertilizations peaked 24–48 hours after the single EPC, and offspring survival to maturity was predicted by parental compatibility rather than by whether the sire was the social or the extra-pair male. The authors concluded that female multiple mating combined with genetically loaded sperm competition lets females target compatible genes — a prominent proposed resolution of the female-infidelity controversy.

The experiment itself, however, could not say which process produced the bias, and the paper explicitly flagged this and related limits: the number of sperm inseminated by each male was not measured, so strategic male sperm allocation could not be excluded; sperm viability across morph combinations and ejaculate × female-tract interactions were not assayed; the strength of compatibility-driven selection in natural populations, and the frequency and precise timing of EPCs in the wild, were unknown; generality to other taxa (inbreeding avoidance, hybridization avoidance, heterosis) was untested; and because heterozygous red males are phenotypically red, pre-copulatory limits on female discrimination could not be separated from post-copulatory selection.

Problem Statement

The problem is to give a complete causal account of compatibility-biased fertilization in the Gouldian finch, comprising two jointly necessary components that share one scientific objective — establishing, mechanistically and ecologically, whether females can and do bias fertilization toward genetically compatible sperm:

(1) Mechanism. Identify which process or combination of processes produces the paternity bias demonstrated by Pryke, Rollins & Griffith (2010): cryptic female choice (female reproductive-tract physiology selectively favouring the sperm of compatible males), strategic male sperm allocation (males adjusting ejaculate size or sperm number to the female's morph), differential sperm viability or performance across morph combinations, or interactions between ejaculate and female-tract genotype. The number of sperm inseminated by each male must be measured or experimentally controlled rather than assumed, so that female-side and male-side alternatives are genuinely separable; morph genotypes must be assigned molecularly, since heterozygous red males are phenotypically indistinguishable from homozygous red males.

(2) Field reality. Determine whether, and with what strength, the process operates in natural populations: quantify extra-pair copulation frequency and timing in the wild and test for compatibility-biased paternity and sex allocation across pairing combinations, resolving whether compatibility-biased fertilization is genuinely absent in the wild, operates at a strength below the detection threshold already achieved by Bolton et al. (2017), or is an artifact of the genetically divergent domesticated stock used in the original experiments.

Cross-taxon generality — whether analogous postcopulatory targeting of compatible genes operates in other taxa, for example in avoiding inbreeding, avoiding hybridization, or realizing heterosis, with designs that separate postcopulatory compatibility selection from pre-copulatory assessment limits and from non-compatibility explanations such as fertility insurance — is related background; it is not a required component of a complete answer to this problem.

References

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