Selection on non-random fusion of gametes during the evolution of anisogamy.
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BACKGROUND: The evolution of differences in gamete size and number between sexes is a cornerstone of sexual selection theories. The green macroalga Ulva, with incipient anisogamy and parthenogenetic gametes, provides a unique system to investigate theoretical predictions regarding the evolutionary pressures that drive the transition from isogamy to anisogamy, particularly in relation to gamete size differentiation and sexual selection. Its minimal gamete dimorphism and facultative parthenogenesis enable a rare window into early evolutionary steps toward anisogamy. RESULTS: By analyzing the expression profiles of sex-biased genes (SBGs) during gametogenesis, we found that SBGs evolve faster than unbiased genes, driven by higher rates of non-synonymous substitution (dN), indicating that SBGs are under stronger selective pressures. Mating type minus-biased genes (mt-BGs) exhibit higher dN/dS values than mating type plus-biased genes (mt+BGs), suggesting stronger selective pressures on mt-BGs, although this difference was not statistically significant (P = 0.08). Using branch-site and RELAX models, we found positive selection and relaxed purifying selection acting on a significant proportion of SBGs, particularly those associated with flagella function. CONCLUSIONS: This study highlights the selective pressures shaping anisogamy and provides insights into the molecular mechanisms underlying its evolution. The faster evolution of SBGs, particularly mt-BGs, and the positive selection on genes associated with motility, such as those related to flagella function, suggest the importance of enhanced gamete motility in the transition to anisogamy. These findings contribute to our understanding of sexual selection and the evolutionary forces that drive the differentiation of gamete size and number between sexes.
Most multicellular animals practice anisogamy (fertilization between eggs and sperm). When mothers produce sons and daughters at a 1:1 ratio, the "twofold cost of males" arises because males do not directly contribute to population growth. If thelytokous parthenogens producing only daughters invade a population, they should spread rapidly. Although thelytoky has repeatedly evolved across invertebrate and vertebrate taxa, it remains a minority. Why? The evolutionary transition from anisogamy to thelytoky requires eggs to initiate embryonic development without fertilization. However, in metazoan animals, meiotic metaphase (MM) arrest halts oogenesis midway and normally resumes only after stimulation by sperm penetration. Empirical and experimental evidences indicate that release of MM arrest without fertilization is extremely difficult, providing a strong mechanistic barrier against parthenogenesis. Even if MM arrest were released, oogenesis would proceed to produce either a haploid embryo or a diploid embryo through refusion with the second polar body (terminal fusion automixis). Outbred species typically accumulate more than one lethal equivalent of recessive deleterious alleles per genome as heterozygotes. Upon transition to haploid or automictic development, these recessive lethals normally masked in outbred diploids would be exposed simultaneously, causing embryonic death and creating the next barrier. Thus, thelytoky cannot be achieved simply by modification of the existing meiotic system; instead, other mechanisms, such as apomixis, that bypass meiosis are required. Mathematical models and simulations support this "meiotic constraint" hypothesis. Combined with recently proposed immediate benefits of anisogamy and traditional genetic benefits (e.g., Red Queen), it may largely explain the maintenance of costly anisogamy.