Evolution of intra-ejaculate sperm interactions: do sperm cooperate?

Abstract

Sperm are often considered to be individuals, in part because of their unique genetic identities produced as a result of synapsis during meiosis, and in part due to their unique ecology, being ejected away from the soma to continue their existence in a foreign environment. Selection at the level of individual sperm has been suggested to explain the evolution of two enigmatic sperm phenotypes: sperm heteromorphism, where more than one type of sperm is produced by a male, and sperm conjugation, where multiple sperm join together for motility and transport through the female reproductive tract before dissociation prior to fertilization. In sperm heteromorphic species, only one of the sperm morphs typically participates in fertilization, with the non-fertilizing "parasperm" being interpreted as reproductive altruists. Likewise, in species with sperm conjugation, high levels of sperm mortality have been suggested to be required for conjugate break-up and this has been considered evidence of kin-selected altruism. However, it is unclear if sperm possess the heritable variation in fitness (i.e. are individuals) required for the evolution of cooperation. We investigate the question of sperm individuality by focusing on how sperm morphology is determined and how sperm conjugates are formed. Concentrating on sperm conjugation, we discuss functional hypotheses for the evolutionary maintenance of this remarkable trait. Additionally, we speculate on the potential origins of sperm heteromorphism and conjugation, and explore the diversification and losses of these traits once they have arisen in a lineage. We find current evidence insufficient to support the concept of sperm control over their form or function. Thus, without additional evidence of haploid selection (i.e. sperm phenotypes that reflect their haploid genome and result in heritable differences in fitness), sperm heteromorphism and conjugation should be interpreted not as cooperation but rather as traits selected at the level of the male, much like other ejaculatory traits such as accessory gland proteins and ejaculate size.

Sperm variation within a single ejaculate affects offspring development in Atlantic salmon

“…First, the empirical evidence for haploid gene expression is growing [13,14], suggesting that we may need to re-evaluate the possibility that translation of the haploid set of genes within a sperm affects sperm phenotypes and is correlated with offspring performance [15][16][17]. However, haploid gene expression in animals is highly debated [17]. Second, preand postmeiotic sperm senescence [18,19] in conjunction with the production of ejaculates with mixed-aged sperm could generate a relationship between sperm performance and mutational load in individual sperm.…”

An Analytical Framework for Estimating Fertilization Bias and the Fertilization Set from Multiple Sperm-Storage Organs

“…The log transformations of the Eggert et al (2003) model can help restore normality to the regression of on , but they S1/S2 1/P 2 necessitate nonzero values for N1 and N2. Using maximum likelihood methods, Neff and Wahl (2004) proposed a nonlinear solution that additionally incorporates a measure of economy of scale, t, quantifying disproportionate returns to number of sperm, such as in cases of sperm conjugation (Higginson and Pitnick 2011). They also redefine r as a bias relative to the second male's sperm, to be consistent with the focus on P 2 (Neff and Wahl 2004; also see Eggert et al 2003):…”

Sperm wars and the evolution of male fertility

“…Cooperation among sperm within a given male's ejaculate is another exciting area of research in sperm competition that deserves greater attention (Pizzari & Foster 2008, Higginson & Pitnick 2010. In a variety of species, sperm can form conjugates of two or more individuals, who collectively swim faster than can Sperm wars individual sperm (Hayashi 1998, Moore et al 2002, Fisher & Hoekstra 2010.…”

“…Nonetheless, experimental evolution failed to find divergence in the curvature of the sperm hook among populations of house mice experiencing variation in the strength of selection from sperm competition (Firman & Simmons 2009, Firman et al 2011. The evolution of cooperation among sperm in the race to fertilize ova will depend strongly on whether sperm are under individual haploid control or whether they are controlled by the diploid male producing them (Immler 2008, Pizzari & Foster 2008, Higginson & Pitnick 2010). …”