Opinion
Embryo Selection and Mate Choice: Can ‘Honest Signals’ Be Trusted?

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Highlights

  • Mate choice by honest signaling is a classic explanation for elaborate traits in nature. Many researchers have: (i) observed deceptive signaling, and (ii) wondered how honest signals relate to trait elaboration.

  • Honest signaling is analogous to high-stakes testing. Quality is hard to measure directly, so proxies (tests) are used. High-stakes testing causes ‘teaching to the test’ without improving educational outcomes.

  • Embryo choice is another high-stakes test. Mothers select healthy embryos and terminate sub-par embryos automatically. Embryos are selected to pass maternal tests without improving their quality. The resulting arms race causes extreme and elaborate signals during pregnancy.

  • We can better understand elaborate traits in nature if we interpret mate selection, and embryo choice, as a dynamic give-and-take between two parties with conflicting fitness interests.

When a measure becomes a target, it often ceases to be a good measure – an effect familiar from the declining usefulness of standardized testing in schools. This economic principle also applies to mate choice and, perhaps surprisingly, pregnancy. Just as females screen potential mates under many metrics, human mothers unconsciously screen embryos for quality. ‘Examinees’ are under intense selection to improve test performance by exaggerating formerly ‘honest’ signals of quality. Examiners must change their screening criteria to maintain useful information (but cannot abandon old criteria unilaterally). By the resulting ‘proxy treadmill’, new honest indicators arise while old degraded indicators linger, resulting in trait elaboration and exaggeration. Hormone signals during pregnancy show extreme evolutionary escalation (akin to elaborate mating displays).

Section snippets

If the Stakes Are High, Measurement Is Hard

High-stakes testing is meant to measure performance in many contexts, but it also causes systemic, and unwanted behavior change. Often the things tested are easily measured proxies (e.g., standardized test scores at a middle school) for more difficult-to-measure attributes (e.g., how well the middle school teachers educate their pupils). Teachers ‘teach to the test’ rather than improving students’ reading skills [1]. Poorly performing students are sometimes encouraged to stay home [2,3]. In a

Choosing a Partner: The Displaying Sex Has Incentives to ‘Cheat’, but Some Forces Resist

In mate choice, members of one sex, usually females, assess the performance of the other sex in a mating display. Multiple selective pressures interact to shape female preference and favor particular male traits, including sensory bias (pre-existing preference for particular traits [14,15]), arbitrary aesthetic preferences [16., 17., 18., 19., 20.], and the need to identify members of one’s own species [21]; however, the most common explanation is that females use display traits to select a

The Proxy Treadmill: New Honest Signals Evolve and Degraded Signals Linger

Observable proxies are chosen because they correlate with more difficult-to-observe qualities. However, this correlation tends to weaken because the proxy becomes a direct target of selection for test-taking ability. This can be thought of as ‘sensory manipulation’ of the examiner by the examinee. If examiners are to continue to select higher-quality examinees, they must seek new proxies that are better correlates of desired qualities. However, there is a conservative force, recognized by

Choosing a Child: Signal Elaboration by the Proxy Treadmill during Human Pregnancy

One rationale for ‘honest signaling’ or ‘good genes’ models of mate choice is that females select males based on the expected quality of their genetic contribution to offspring. This is indirect selection of offspring: a high-quality male may father some low-quality offspring because of the vagaries of genetic recombination and epistatic interactions between maternal and paternal genomes. A more direct way to improve the quality of offspring would be to examine offspring themselves before major

Concluding Remarks: Why Are Placentas Like Birds-of-Paradise?

Placentas must achieve a simple task: passing goods between mother and fetus. It should be a piece of cake. But placentas are wildly diverse across mammals, ‘evolving and experimenting at a disturbingly rapid pace’ [47], reminiscent of the bizarre diversity of birds-of-paradise [64]. Pregnancy in placental mammals is a case of antagonistic coevolution between signaler and receiver. The sensory onslaughts of placental hormones in embryo choice, and fantastic ornaments in mate choice, are

Acknowledgments

We are very grateful to two anonymous reviewers for their feedback. We would like to thank John Christy for particularly useful feedback, including suggesting the terminology ‘aesthetic residue’ and suggesting multiple specific predictions and outstanding questions. We are grateful to Arvid Ågren, Pavitra Muralidhar, Carl Veller, and Inbar Mayaan for comments on the manuscript. D.E.M.’s research is conducted with Government support under and awarded by DoD, Air Force Office of Scientific

Glossary

Aesthetic residue
display trait which is no longer indicative of quality but is nonetheless retained in signaler–displayer examinations because it would be costly to abandon.
Campbell’s law
a principle in social sciences that states that quantitative proxies, or metrics, meant to measure complicated phenomena are subject to corruption when the indicator is used for decision-making. ‘When a measure becomes a target it ceases to be a good measure.’
Chorionic gonadotropin (CG)
hormone produced by the

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