A model for the origin of heterospory

doi:10.1016/S0022-5193(88)80203-0

Journal of Theoretical Biology

Volume 134, Issue 2, 21 September 1988, Pages 257-272

https://doi.org/10.1016/S0022-5193(88)80203-0 Get rights and content

Sporophytes are predicted to produce spores of a size that maximizes the return in gametophyte fitness per unit investment. Larger spores are predicted for those species in which gametophytes depend on stored food reserves for successful reproduction. A model for the origin of heterospory is proposed, in which an initially homosporous population is subject to natural selection for increased spore size. Because the minimum costs of male reproduction are less than the minimum costs of female reproduction, larger food reserves evolve principally for the use of female reproduction. Above some critical spore size, the population can be invaded by sporophytes producing smaller spores, which reproduce predominantly as males. This model for the origin of heterospory has three phases: (1) a gradual increase of spore size in a homosporous population; (2) the sudden introduction of smaller microspores; (3) the subsequent divergence in size and specialization of the two spore types. The model explains haploid dioecy as a consequence of pre-existing mechanisms of sex determination, and endosporic development as a consequence of an increased dependence on spore food reserves for reproduction.

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Cited by (21)

A dynamical model for the origin of anisogamy
2021, Journal of Theoretical Biology
Citation Excerpt :
“Anisogamy” refers to the observation that gamete size distributions in many species are bimodal or multimodal, and has long been a topic of study (see, e.g., Kalmus, 1932; Kalmus and Smith, 1960; Scudo, 1967; Parker et al., 1972; Bell, 1978; Cox and Sethian, 1985; Hurst, 1990; Bonsall, 2006; Blute, 2013; Lehtonen et al., 2016). Anisogamy is common in complex organisms such as plants, animals, fungi, and certain algae (Parker et al., 1972; Haig and Westoby, 1988; Billiard et al., 2011; Bateman and DiMichele, 1994). There is a consensus in the literature that anisogamy evolved from isogamy, where sexual reproduction occurs between sex cells that are the same size (Parker et al., 1972; Bell, 1978; Bulmer and Parker, 2002; Hayward and Gillooly, 2011).
The vast majority of multi-cellular organisms are anisogamous, meaning that male and female sex cells differ in size. It remains an open question how this asymmetric state evolved, presumably from the symmetric isogamous state where all gametes are roughly the same size (drawn from the same distribution). Here, we use tools from the study of nonlinear dynamical systems to develop a simple mathematical model for this phenomenon. Unlike some prior work, we do not assume the existence of mating types. We also model frequency dependent selection via “mean-field coupling,” whereby the likelihood that a gamete survives is an increasing function of its size relative to the population’s mean gamete size. Using theoretical analysis and numerical simulation, we demonstrate that this mean-referenced competition will almost inevitably result in a stable anisogamous equilibrium, and thus isogamy may naturally lead to anisogamy.
Evolution of development of pollen performance
2019, Current Topics in Developmental Biology
Citation Excerpt :
Fernando (2014) noted that the exceptional year-long progamic phases of conifers likely have a strong genetic basis, because their long developmental sequences are maintained in several derived lineages that have transitioned from temperate to tropical environments (where long winter dormant periods for pollen tubes would seem to be unwarranted). The reconstruction of ancestrally long progamic phase duration is consistent with the fact that gametophytes in extant seed plant outgroups are perennial or take many months between spore dispersal and the formation of sperm in antheridia (Haig & Westoby, 1988; Lloyd & Klekowski, 1970). Thus, we argue caution in interpreting gymnosperm progamic phases as being “delayed,” when in fact the opposite may be true.
With the origin of pollination in ancient seed plants, the male gametophyte (“pollen”) began to evolve a new and unique life history stage, the progamic phase, a post-pollination period in which pollen sexual maturation occurs in interaction with sporophyte-derived tissues. Pollen performance traits mediate the timing of the fertilization process, often in competition with other pollen, via the speed of pollen germination, sperm development, and pollen tube growth. Studies of pollen development rarely address the issue of performance or its evolution, which involves linking variation in developmental rates to relative fitness within populations or to adaptations on a macroevolutionary scale. Modifications to the pollen tube pathway and changes in the intensity of pollen competition affect the direction and strength of selection on pollen performance. Hence, pollen developmental evolution is always contextual—it involves both the population biology of pollen reaching stigmas and the co-evolution of sporophytic traits, such as the pollen tube pathway and mating system. For most species, performance evolution generally reflects a wandering history of periods of directional selection and relaxed selection, channeled by developmental limitations, a pattern that favors the accumulation of diversity and redundancy in developmental mechanisms and the genetic machinery. Developmental biologists are focused on finding universal mechanisms that underlie pollen function, and these are largely mechanisms that have evolved through their effects on performance. Here, we suggest ways in which studies of pollen performance or function could progress by cross-fertilization between the “evo” and “devo” fields.
Rhabdosporites langii, Geminospora lemurata and Contagisporites optivus: An origin for heterospory within the progymnosperms
1996, Review of Palaeobotany and Palynology
A major mid-Devonian floral event is the incoming and proliferation of the archaeopteridalean progymnosperms. They are generally accepted to have originated from the aneurophytalean progymnosperms. The spores from both groups (the microspore Geminospora lemurata and its megaspore Contagisporites optivus—Archaeopteridales; Rhabdosporites langii—Aneurophytales) are well represented in the Orcadian Basin, Scotland. Study of a long section in southern Orkney shows that G. lemurata first occurs not by progressive size reduction of R. langii but as a small thick-walled spore (“early form”) which is presumed to originate by heterochrony directly from an immature Rhabdosporites. It then progressively increases in size. This early stage of evolution can be timed using the lacustrine cyclicity. Subsequently a rapid increase in abundance occurs with G. lemurata replacing R. langii as the dominant element of the palynofloras. Originating after the first appearance of G. lemurata are spores transitional in morphology between R. langii and C. optivus indicating the progressive development of the megaspore. These changes together with the presence of a three-walled species of Rhabdosporites (Rhabdosporites streelii Marshall, sp. nov.) give a hint of the complex changes occurring within the sporangia of the archaeopteridalean group at this time. These changes show how detailed investigation of related spore taxa can reveal the pattern of the development of heterospory in the Progymnosperms. This permits for the first time a test of the theoretical models for the development of heterospory. The recognition that an “early form” of G. lemurata exists indicates that some caution should be exercised in using the first occurrence of this species as a stratigraphic marker. Rhabdosporites parvulus is confirmed as a small R. langii but the bulk of specimens formerly attributed to this species are G. lemurata. The means that the Eday Group sediments of Orkney are contemporaneous with the Devonian deposits of southeast Shetland and Fair Isle.
Plant paleoecology and evolutionary inference: Two examples from the Paleozoic
1996, Review of Palaeobotany and Palynology
Paleobotany can contribute much to evolutionary scenario-building. Here, we use two case studies — the Devono-Carboniferous vascular plant radiation and the largely coeval evolution of heterosporous from homosporous life histories — to examine the interface between phylogeny and ecology. Our observations challenge some tenets of the neo-Darwinian orthodoxy, notably the assumed role of competition mediated selection as an active driving force, rather than a passive filter, of evolution.
The Devono-Carboniferous class-level radiation of vascular plants was prompted by attainment of a complexity threshold and delimited the morphological envelope that enclosed an apparently fractal pattern of subsequent, lower level radiations. The contrast of low speciation rates with exceptionally high rates of phenotypic divergence in the Devonian suggests a non-adaptive “novelty” radiation, perhaps reflecting saltational evolution via “hopeful monsters”. Successive lower level radiations were more constrained by the ecological hierarchy that resulted from progressive niche differentiation and saturation. This in turn reflected increased speciation rates, thereby completing a well defined negative feedback loop in the coevolution of phenotypic and ecological differentiation.
Heterosporous life histories evolved independently in at least ten lineages. Heterospory allows the sporophyte to impose, via differential development, a single fixed gender on each gametophyte prior to spore release. Although the resulting life history is less flexible than homospory, which on recent evidence includes a range of subtle and sophisticated strategies, it promotes the sporophyte as the primary target for selection. Gametophytes effectively perform the role of gametes and are released into the environment prior to fertilization, thus favoring aquatic—amphibious habitats resistant to occupation by homosporous pteridophytes; terrestrial heterospory requires apomixis. Although the profound iteration of heterospory implies a strong adaptive advantage, repeated gradual evolution via inferior intermediates exhibiting exosporous heterospory seems unlikely.
Seed-plant success reflects economic efficiency and the subsequent evolution of effective pollination syndromes, rather than integumentation of the ovule. Major radiations of heterosporous lineages and subsequently of seed-plants required perturbation of pre-existing communities by extrinsic environmental changes rather than genuinely competitive displacement. This typical manifestation of “home-field advantage” further emphasizes the intimate relationship between phylogeny and ecology, and allows us to make predictions that can be tested by further paleobotanical research.
Understanding the appearance of heterospory and derived plant reproductive strategies in the Devonian
2022, Paleobiology
A Dynamical Model for the Origin of Anisogamy
2021, arXiv

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^*: This paper is dedicated to the memory of Rudolf Lemberg who encouraged one of us (Haig) in an early interest in biology.

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A model for the origin of heterospory*

J. theor. Biol.

Rev. Palaeobotany Palynol.

J. theor. Biol.

J. theor. Biol.

J. theor. Biol.

J. theor. Biol.

Ecology

The Theory of Sex Allocation

Amer. Nat.

Bot. J. Linn. Soc.

Pollen and Spore Morphology/Plant Taxonomy, Vol. IV

Bot. Rev.

Ann. Rev. Ecol. Syst.

Amer. J. Bot.

Bot. J. Linn. Soc.

Bot. J. Linn. Soc.