“Evolution of the two sexes under internal fertilization and alternative evolutionary pathways”

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Jussi Lehtonen and Geoff A. Parker (May 2019)

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Anisogamy theory is robust under internal fertilization and sperm packets, bridging gap between theory and empirical tests

Broadening our theoretical understanding of the evolutionary origin of the two sexes

Biologically, the two sexes are defined by the size of their gametes. Females are by definition the type that produces the larger gametes (e.g. eggs) and males the type that produces the smaller gametes (e.g. sperm). In this sense the origin of gamete size dimorphism is synonymous with the origin of the two sexes. Our understanding of this major event in evolutionary history is largely based on so-called gamete dynamics theory, where there are simultaneous selective pressures driving selection for numerous (hence small) and large (hence less numerous) gametes. Small and numerous gametes are good at gaining fertilizations, while large gametes are good at provisioning offspring. Although empirical evidence is fairly supportive of this theory, much of the evidence comes from organisms with simple forms of internal fertilization, while the original theory is derived for external fertilizers. Furthermore, some of these organisms divide their gametes into ‘sperm packets’, further increasing the divide between theory and data. In a new article, Jussi Lehtonen of the University of Sydney, Australia, and Geoff Parker of the University of Liverpool, UK, generalize previous theory on the origin of the two sexes, showing that the theory works equally well under the biology of these model organisms. Hence gamete dynamics theory represents a potent rationale for the origin of the two sexes.


Abstract

Transition from isogamy to anisogamy, hence males and females, leads to sexual selection, sexual conflict, sexual dimorphism, and sex roles. Gamete dynamics theory links biophysics of gamete limitation, gamete competition and resource requirements for zygote survival, and assumes broadcast spawning. It makes testable predictions, but most comparative tests use volvocine algae, which feature internal fertilization. We broaden this theory by comparing broadcast spawning predictions with two plausible internal fertilization scenarios: gamete-casting/brooding (one mating type retains gametes internally, the other broadcasts them) and packet-casting/brooding (one type retains gametes internally, the other broadcasts packets containing gametes, which are released for fertilization). Models show that predictions are remarkably robust to these radical changes, yielding (i) isogamy under low gamete limitation, low gamete competition, and similar required resources for gametes and zygotes, (ii) anisogamy when gamete competition and/or limitation are higher, and when zygotes require more resources than gametes, as is likely as multicellularity develops, (iii) a positive correlation between multicellular complexity and anisogamy ratio, and (iv) under gamete competition, only brooders becoming female. Thus gamete dynamics theory represents a potent rationale for isogamy/anisogamy, and makes similar testable predictions for broadcast spawners and internal fertilizers, regardless of whether anisogamy or internal fertilization evolved first.