Comparative analysis of the largest vertebrate testes-mass dataset to date revealed explosive, clade-specific bursts of relative testes-mass evolution throughout 400 million years of vertebrate history, and a unique pattern in birds: repeated rapid directional reductions in relative testes mass specifically along lineages evolving social monogamy, seen in no other vertebrate group. What remains unresolved is the mechanism: how changes in social mating system produce the observed radiations of testes-mass diversity, and why the sustained directional reduction occurs only in monogamous birds. Competing explanations — energy-allocation trade-offs with other costly traits, a secular decline in sperm competition within monogamous lineages, and the exceptional prevalence of social monogamy combined with internal fertilization in birds — remain untested at macroevolutionary scale, and large-scale data linking genetic measures of multiple paternity to social mating systems are only now becoming available.

Background

Sperm competition — competition between sperm of different males to fertilize a female's eggs — is a major driver of male reproductive morphology: larger testes produce more sperm and improve fertilization success when females mate with multiple males. Across species, testes mass therefore scales with body mass, and deviations from this allometric line (relative testes mass, typically the residual or phylogenetically corrected contrast of log testes mass against log body mass) indicate investment in sperm production relative to a species' size. Social mating system — the number of sexual partners an individual forms pair bonds or social associations with (monogamy, polyandry where females associate with multiple males, polygyny where males associate with multiple females) — is widely used as a proxy for the intensity of sperm competition, but only imperfectly: in socially monogamous birds, genetic paternity analysis frequently shows that offspring are sired by males outside the pair bond (extra-pair paternity, EPP), so the social and genetic mating systems need not coincide. Baker, Humphries, Ferguson-Gow, Meade and Venditti (2020, Ecology Letters 23:283–292) combined a dataset of testes masses spanning the vertebrate tree with Bayesian phylogenetic methods that estimate how fast a trait has evolved along each branch of the evolutionary tree (rate heterogeneity). They found that testes-mass diversity arose in repeated bursts of rapid change distributed across vertebrate phylogeny — for example in polyandrous rhacophorid tree frogs, the monogamous California mouse, hopping mice of the genus Notomys, and pipefish — rather than by gradual accumulation. Strikingly, when rapid change was directional (a consistent trend toward larger or smaller values), that direction was almost always toward smaller testes, and only in one setting: birds with social monogamy, where sperm competition is lowest. No other vertebrate group showed sustained directional testes-mass evolution in association with any mating system. The authors rejected one candidate explanation for the avian uniqueness — the restricted energy budget of flight — because bats, the other flying vertebrates, show no such directionality. The remaining candidate explanations are: (i) trade-offs with other expensive tissues or behaviors, since investment in ornaments, weapons, or parental care may pay off more than testes when sperm competition is low (a macroevolutionary version of the expensive-tissue logic that costly organs compete for a finite energy budget); (ii) a continuing decline in the level of sperm competition within monogamous bird lineages over time; and (iii) the fact that birds are exceptional among vertebrates in combining very high prevalence of social monogamy (over 75% of species) with internal fertilization, which may open ecological space for alternative investments. Each hypothesis was stated but not tested. A further obstacle is that social mating system is an imperfect proxy for actual sperm competition: existing genetic measures of multiple paternity (EPP frequency, extra-group paternity, number of sires per brood) are not clearly comparable across social systems, and at the time no dataset linked them to social systems at large taxonomic scale.

Problem Statement

Identify and empirically support the mechanism(s) by which changes in social mating system have produced the observed pattern of vertebrate testes-mass evolution, making the social-mating-system-to-testes-rate link explicit and quantitatively testable at macroevolutionary scale — specifically: (1) explain why repeated rapid directional reductions in relative testes mass have occurred only in socially monogamous birds and in no other vertebrate group, discriminating among the candidate explanations of energy-allocation trade-offs with other costly traits or behaviors, a secular decline in sperm competition levels within monogamous lineages, and the joint exceptional prevalence of social monogamy and internal fertilization in birds — ranking the relative support for each and stating which, if any, can be excluded; and (2) determine how transitions between social mating systems map mechanistically onto the repeated clade-specific bursts of rapid relative-testes-mass change detected throughout the vertebrate tree, including which drivers (sperm competition itself versus covariates such as geography, dispersal, mating rate, and migratory behavior) account for the rate heterogeneity.

References

  1. Baker J, Humphries S, Ferguson-Gow H, Meade A, Venditti C (2020) Rapid decreases in relative testes mass among monogamous birds but not in other vertebrates. Ecology Letters 23(2):283–292. DOI: 10.1111/ele.13431. https://doi.org/10.1111/ele.13431
  2. Baker J, Meade A, Venditti C (2021) Genes underlying the evolution of tetrapod testes size. BMC Biology 19:162. DOI: 10.1186/s12915-021-01107-z. https://doi.org/10.1186/s12915-021-01107-z
  3. Valencia-Aguilar A, Ringler E, Lüpold S, Guayasamin JM, Prado CPA (2024) Evolutionary trade-offs between testes size and parenting in Neotropical glassfrogs. Proceedings of the Royal Society B 291:20240054. DOI: 10.1098/rspb.2024.0054. https://doi.org/10.1098/rspb.2024.0054
  4. Koçillari L, Cattelan S, Rasotto MB, Seno F, Maritan A, Pilastro A (2024) Tetrapod sperm length evolution in relation to body mass is shaped by multiple trade-offs. Nature Communications 15:6160. DOI: 10.1038/s41467-024-50391-0. https://doi.org/10.1038/s41467-024-50391-0
  5. Alexander A, Iglesias-Carrasco M, Lozano M, Garcia-Gonzalez F (2025) Monogamy removes constraints on reproductive tissue investment imposed by intense sexual selection. Scientific Reports 15:19646. DOI: 10.1038/s41598-025-00180-6. https://doi.org/10.1038/s41598-025-00180-6
  6. Barber RA, Yang J, Yang C, Barker O, Janicke T, Tobias JA (2024) Climate and ecology predict latitudinal trends in sexual selection inferred from avian mating systems. PLoS Biology 22(11):e3002856. DOI: 10.1371/journal.pbio.3002856. https://doi.org/10.1371/journal.pbio.3002856
  7. Dobson FS, Correia HE, Abebe A (2024) How much multiple paternity should we expect? A study of birds and contrast with mammals. Ecology and Evolution 14(3):e11054. DOI: 10.1002/ece3.11054. https://doi.org/10.1002/ece3.11054