Pollen and sperm heteromorphism: convergence across kingdoms?

Abstract

Sperm competition theory predicts that males should produce many, similar sperm. However, in some species of animals and plants, males exhibit a heteromorphism that results in the production of at least two different types of sperm or pollen grains. In animals, sperm heteromorphism typically corresponds to the production of one fertile morph and one (or more) sterile morph(s), whereas in plants two or more pollen morphs (one of which can be either sterile or fertile) are produced in all flowers but sometimes in different anthers. Heteromorphism has arisen independently several times across phyla and at different phylogenetic levels. Here, we compare and contrast sperm and pollen heteromorphism and discuss the evolutionary hypotheses suggested to explain heteromorphism in these taxa. These hypotheses include facilitation, nutritive contribution, blocking, cheap filler, sperm flushing or killing for animals; outcrossing and precise cross‐pollen transfer or bet‐hedging strategy for plants; cryptic female choice for both. We conclude that heteromorphism in the two phyla is most likely linked to a general evolutionary response to sexual selection, either to increase one male's sperm or pollen success in competition with other males, or mediate male/female interactions. Therefore, although sperm and pollen are not homologous, we suggest that heteromorphism represents an example of convergence across kingdoms.

Pollen aperture heteromorphism inCentaurium pulchellum(Gentianaceae)

“…Pollen aperture variability is frequently associated with heterostyly or zygomorphy (Till-Bottraud et al, 2005) and is related to breeding systems or pollination strategy (Punt et al, 1974;Mignot et al, 1994;Barrett, 2002). Nevertheless, the development of pollen heteromorphism is not clearly understood, and remains a subject of discussion.…”

Sperm wars and the evolution of male fertility

“…Indeed, there are many examples of species that produce heteromorphic sperm, which in animals typically results in the production of both fertile and non-fertile sperm morphs (Till-Bottraud et al 2005). There is evidence from insects that non-fertilizing sperm morphs can control female remating rates (Cook & Wedell 1999) and protect fertilizing sperm from immunological attack from the female's reproductive tract .…”

Sperm competition and sperm cooperation: the potential role of diploid and haploid expression

“…The extreme case of phenotypic and functional variation among sibling sperm is sperm heteromorphism, where a male's ejaculate contains fertile and non-fertile sperm, and which is found in different phyla including plants, arthropods, molluscs and vertebrates (Snook 2005, Till-Bottraud et al 2005. Sperm heteromorphism may reduce the competition among sibling sperm due to the clear division of labour between fertilising and nonfertilising sperm, which may differ considerably in shape and function.…”

“…However, the costs may differ relatively for sperm and for the male: from empirical evidence, it appears that sperm cooperation often involves the loss of fertilisation capability of some sperm (e.g. , Till-Bottraud et al 2005. In this case, the costs are potentially much higher for sperm than for the male: sperm destroy themselves for the benefit of sibling sperm (Zcosts are 100%), whereas the male loses a certain amount of sperm, yet even if sperm production is costly, the cost to the male is relatively small compared with the cost to the sperm.…”