Plant-like mating in an animal: sexual compatibility and allocation trade-offs in a simultaneous hermaphrodite with remote transfer of sperm

Abstract

The importance of sexual compatibility between mates has only recently been realized in zoological research into sexual selection, yet its study has been central to botanical research for many decades. The reproductive characteristics of remote mating, an absence of precopulatory mate screening, internal fertilization and embryonic brooding are shared between passively pollinated plants and a phylogenetically diverse group of sessile aquatic invertebrates. Here, we further characterize the sexual compatibility system of one such invertebrate, the colonial ascidian Diplosoma listerianum. All 66 reciprocal pairings of 12 genetic individuals were carried out. Fecundities of crosses varied widely and suggested a continuous scale of sexual compatibility. Of the 11 animals from the same population c. 40% of crosses were completely incompatible with a further c. 20% having obvious partial compatibility (reduced fecundity). We are unaware of other studies documenting such high levels of sexual incompatibility in unrelated individuals. RAPD fingerprinting was used to estimate relatedness among the 12 individuals after a known pedigree was successfully reconstructed to validate the technique. In contrast to previous results, no correlation between genetic similarity and sexual compatibility was detected. The blocking of many genotypes of sperm is expected to severely modify realized paternity away from ‘fair raffle’ expectations and probably reduce levels of intra‐brood genetic diversity in this obligatorily promiscuous mating system. One adaptive benefit may be to reduce the bombardment of the female reproductive system by outcrossed sperm with conflicting evolutionary interests, so as to maintain female control of somatic : gametic investment.

Effects of competition on sexual and clonal reproduction of a tunicate: the importance of competitor identity

“…The resulting loss of space from overgrowth and consequent death of part of the colony affects both asexual and sexual reproduction. Alternative strategies of growth in the face of competition also affect how species occupy space, and appear to result in a 3-way tradeoff in resource allocation between asexual reproduction and male and female function (Williams 1975, Stocker & Underwood 1991, Yund et al 1997, Newlon et al 2003, Pemberton et al 2004, Tarjuelo & Turon 2004, López-Legentil et al 2005. For example, the soft coral, Efflatounaria sp., has a variable life-cycle strategy: at low densities, stolons facilitate rapid directional growth, whereas at high densities, stolons are inhibited, but mortality rates are greatly reduced (Karlson et al 1996).…”

Sexual Conflict in Hermaphrodites

“…A number of potential mechanisms for cryptic female choice have been proposed. These include the differential storage and usage of sperm from multiple sperm storage tubules (Baur 2007; but see Koemtzopoulos and Staikou 2007), the postmating "suck" behavior of M. lignano already mentioned above (Schärer et al 2004;Vizoso et al 2010;Marie-Orleach et al 2013), and the blocking and phagocytosis of received self-sperm and certain allosperm in the oviduct, and thus preferential fertilization by allosperm from "preferred" clones in the spermcasting ascidian Diplosoma listerianum (Bishop 1996;Bishop et al 1996;Pemberton et al 2004). Sperm recipients may also retain more control of sperm uptake, and hence paternity outcomes, when transfer occurs via the external exchange of spermatophores (e.g., in the nudibranch Aeolidiella glauca) (Haase and Karlsson 2000;Karlsson and Haase 2002; see also Bishop and Pemberton 2006).…”

Lessons in modularity: the evolutionary ecology of colonial invertebrates

“…D. listerianum on the other hand discriminates not only against autosperm but also among unrelated allosperm sources Pemberton et al, 2004). Fitness advantages of mate choice beyond kinship are unknown in colonial invertebrates, but might include heterozygous advantage (Saavedra and Guerra, 1996), dominance in cell-lineage competition (Stoner et al, 1999) and in spermcasters such as D. listerianum, female control of somatic-gametic investment (Pemberton et al, 2004).…”

“…Spermcast mating may be an evolutionary solution to such problems common to diverse sessile invertebrates, which as shown in D. listerianum and C. hyalina, may be able to take up water-borne sperm entrained in the feeding current and store it for considerable periods (Bishop, 1998;Pemberton et al, 2004). Sperm accumulated in this way are likely to originate from multiple donors, with consequent manifestations of sperm competition and female choice.…”

“…Fitness advantages of mate choice beyond kinship are unknown in colonial invertebrates, but might include heterozygous advantage (Saavedra and Guerra, 1996), dominance in cell-lineage competition (Stoner et al, 1999) and in spermcasters such as D. listerianum, female control of somatic-gametic investment (Pemberton et al, 2004). Rewarding possibilities for studying the evolutionary implications of cryptic mate choice (Cordoba-Aguilar and Contreras- Garduno, 2003) are afforded by the experimental breeding of pedigree clones of colonial invertebrates and the development of suitable genetic markers (Hoare et al, 1998;Craig et al, 2001;Maclean et al, 2004;Pemberton et al, 2004).…”