Geoff A Parker

In eukaryotes, a fundamental phenomenon underlying sexual selection is the evolution of gamete size dimorphism between the sexes (anisogamy) from an ancestral gametic system with gametes of the same size in both mating types (isogamy). The nuclear–cytoplasmic conflict hypothesis has been one of the major theoretical hypotheses for the evolution of anisogamy. It proposes that anisogamy evolved as an adaptation for preventing nuclear–cytoplasmic conflict by minimizing male gamete size to inherit organelles uniparentally. In ulvophycean green algae, biparental inheritance of organelles is observed in isogamous species, as the hypothesis assumes. So we tested the hypothesis by examining whether cytoplasmic inheritance is biparental in Monostroma angicava, a slightly anisogamous ulvophycean that produces large male gametes. We tracked the fates of mitochondria in intraspecific crosses with PCR …

Though the first attempts to introduce game theory into evolutionary biology failed, new formalism by Maynard Smith and Price in 1973 had almost instant success. We use information supplied by early workers to analyse how and why evolutionary game theory (EGT) spread so rapidly in its earliest years. EGT was a major tool for the rapidly expanding discipline of behavioural ecology in the 1970s; each catalysed the other. The first models were applied to animal contests, and early workers sought to improve their biological reality to compare predictions with observations. Furthermore, it was quickly realized that EGT provided a general evolutionary modelling method; not only was it swiftly applied to diverse phenotypic adaptations in evolutionary biology, it also attracted researchers from other disciplines such as mathematics and economics, for which game theory was first devised. Lastly, we pay attention to …

Parasitic worms (helminths) with complex life cycles divide growth and development between successive hosts. Using data from 597 species of acanthocephalans, cestodes, and nematodes with two-host life cycles, we found that helminths with larger intermediate hosts were more likely to infect larger, endothermic definitive hosts, although some evolutionary shifts in definitive host mass occurred without changes in intermediate host mass. Life-history theory predicts parasites to shift growth to hosts in which they can grow rapidly and/or safely. Accordingly, helminth species grew relatively less as larvae and more as adults if they infected smaller intermediate hosts and/or larger, endothermic definitive hosts. Growing larger than expected in one host, relative to host mass/endothermy, was not associated with growing less in the other host, implying a lack of cross-host trade-offs. Rather, some helminth orders had …

An organism's maximum gonad investment (MGI) typically indicates its reproductive season and is often measured by the peak of the gonadosomatic index. Since external sexual dimorphism is often not evident, intrinsic sex differences remain unstudied. We analysed the reproductive seasonality of each sex of the broadcast-spawning sea cucumber Holothuria (Halodeima) inornata in two populations (Caleta de Campos, Michoacán ‘CC’ and Puerto Madero, Chiapas ‘PM’) in the southern coast of the Mexican Pacific by examining: intensity and duration of MGI, frequency of each gonadal developmental stage (GDS) through time, sexual asymmetry in GSI, sexual asymmetry in GDS, and adult sex ratio. We observed a trade-off between the intensity (%) and duration (months) of each sex's MGI: as intensity decreases, duration increases and conversely. The frequency of ripe and spawning stages was consistently …

Why do so many parasitic worms have complex life-cycles? A complex life-cycle has at least two hypothesized costs: (i) worms with longer life-cycles, i.e. more successive hosts, must be generalists at the species level, which might reduce lifetime survival or growth, and (ii) each required host transition adds to the risk that a worm will fail to complete its life-cycle. Comparing hundreds of trophically transmitted acanthocephalan, cestode, and nematode species with different life-cycles suggests these costs are weaker than expected. Helminths with longer cycles exhibit higher species-level generalism without impaired lifetime growth. Further, risk in complex life-cycles is mitigated by increasing establishment rates in each successive host. Two benefits of longer cycles are transmission and production. Longer cycles normally include smaller (and thus more abundant) first hosts that are likely to consume parasite …

Parasitic worms with complex life cycles have several developmental stages, with each stage creating opportunities to infect additional host species. Using a data set for 973 species of trophically transmitted acanthocephalans, cestodes, and nematodes, we confirmed that worms with longer life cycles (i.e., more successive hosts) infect a greater diversity of host species and taxa (after controlling for study effort). Generalism at the stage level was highest for middle life stages, the second and third intermediate hosts of long life cycles. By simulating life cycles in real food webs, we found that middle stages had more potential host species to infect, suggesting that opportunity constrains generalism. However, parasites usually infected fewer host species than expected from simulated cycles, suggesting that generalism has costs. There was no trade-off in generalism from one stage to the next, but worms spent less time …

Shuker and Kvarnemo define sexual selection as non-random fertilization resulting from competition-for-gametes. They remove gender, mate number, resources, and mating system from this polysemous term. Here, definitional economy comes at a price: Utility. Consider two predictions that stem from how such competition and subsequent fertilization manifest themselves:1) Sexual selection arising from gametic competition is expected to result in the mean fitness of fertilizing males (or females) being greater than the mean of all mating males (or females). This outcome is inevitable because with gametic competition, winners will be over-represented, and losers will be under-represented in each generation.

The two sexes are defined by the sizes of the gametes they produce, anisogamy being the state with two differing gamete sizes (hence, females and males). The origin of this divergence has received much research interest, both theoretically and empirically. The gamete dynamics (GD) theory is a widely accepted theoretical explanation for anisogamy, and green algae have been an important empirical testing ground for the theory. However, some green and brown algae produce parthenogenetic gametes (gametes that can develop without fusing with another gamete), in contrast to an assumption in GD theory that unfused gametes do not develop. Here, we construct a GD model accounting for parthenogenetic gametes. We find that under conditions of panmixia and highly efficient fertilization (i.e., conditions of classical GD models from 1972 onward), the results remain largely unaltered by parthenogametes …

Parasitic worms (i.e., helminths) commonly infect multiple hosts in succession. With every transmission step, they risk not infecting the next host and thus dying before reproducing. Given this risk, what are the benefits of complex life cycles? Using a dataset for 973 species of trophically transmitted acanthocephalans, cestodes, and nematodes, we tested whether hosts at the start of a life cycle increase transmission and whether hosts at the end of a life cycle enable growth to larger, more fecund sizes. Helminths with longer life cycles, that is, more successive hosts, infected conspicuously smaller first hosts, slightly larger final hosts, and exploited trophic links with lower predator–prey mass ratios. Smaller first hosts likely facilitate transmission because of their higher abundance and because parasite propagules were the size of their normal food. Bigger definitive hosts likely increase fecundity because parasites …

Gamete dynamics theory proposes that anisogamy arises by disruptive selection for gamete numbers versus gamete size and predicts that female/male gamete size (anisogamy ratio) increases with adult size and complexity. Evidence has been that in volvocine green algae, the anisogamy ratio correlates positively with haploid colony size. However, green algae show notable exceptions. We focus on Bryopsidales green algae. While some taxa have a diplontic life cycle in which a diploid adult (=fully grown) stage arises directly from the zygote, many taxa have a haplodiplontic life cycle in which haploid adults develop indirectly: the zygote first develops into a diploid adult (sporophyte) which later undergoes meiosis and releases zoospores, each growing into a haploid adult gametophyte. Our comparative analyses suggest that, as theory predicts: (i) male gametes are minimized, (ii) female gamete sizes vary …

This review documents the history of the two papers written half a century ago that relate to this special issue of Cells. The first, “Sperm competition and its evolutionary consequences in the insects” (Biological Reviews, 1970), stressed that sexual selection continues after ejaculation, resulting in many adaptations (e.g., postcopulatory guarding phases, copulatory plugs, seminal fluid components that modify female reproduction, and optimal ejaculation strategies), an aspect not considered by Darwin in his classic treatise of 1871. Sperm competition has subsequently been studied in many taxa, and post-copulatory sexual selection is now considered an important sequel to Darwinian pre-copulatory sexual selection. The second, “The origin and evolution of gamete dimorphism and the male-female phenomenon” (Journal of Theoretical Biology, 1972) showed how selection, based on gamete competition between individuals, can give rise to anisogamy in an isogamous broadcast spawning ancestor. This theory, which has subsequently been developed in various ways, is argued to form the most powerful explanation of why there are two sexes in most multicellular organisms. Together, the two papers have influenced our general understanding of the evolutionary differentiation of the two forms of gametic cells, and the divergence of sexual strategies between males and females under sexual selection.

The past half century has seen the development of the field of post-ejaculatory sexual selection, the sequel to sexual selection for mate-acquisition (pre-ejaculatory) described by Darwin. In richness and diversity of adaptations, post-ejaculatory selection rivals that of pre-ejaculatory sexual selection. Anisogamy—and hence two sexes—likely arose by primeval gamete competition, and sperm competition remains a major force maintaining high sperm numbers. The post-ejaculatory equivalent of male–male competition for matings, sperm competition was an intense ancestral form of sexual selection, typically weakening as mobility and internal fertilization developed in many taxa, when some expenditure became diverted into pre-ejaculatory competition. Sperm competition theory has been relatively successful in explaining variation in relative testes size and sperm numbers per ejaculate and is becoming more …

Studies of the yellow dungfly in the 1960s provided one of the first quantitative demonstrations of the costs and benefits associated with male and female reproductive behaviour. These studies advanced appreciation of sexual selection as a significant evolutionary mechanism and contributed to the 1970s paradigm shift toward individual selectionist thinking. Three behaviours in particular led to the realization that sexual selection can continue during and after mating: (i) female receptivity to remating, (ii) sperm displacement and (iii) post-copulatory mate guarding. These behaviours either generate, or are adaptations to sperm competition, cryptic female choice and sexual conflict. Here we review this body of work, and its contribution to the development of post-copulatory sexual selection theory. This article is part of the theme issue ‘Fifty years of sperm competition’.

Grazing mammals, ungulates, pose two evolutionary puzzles as helminth hosts. First, why do some helminths infect intermediate hosts prior to infecting ungulates, given that grazers could directly consume propagules on vegetation? Second, ungulates are large and long-lived, so why are they occasionally intermediate instead of definitive hosts, as in taeniid cestodes? We comprehensively surveyed helminth life cycles and transmission involving ungulates. We identified six transmission routes and found that ungulate helminth parasitism has evolved some 25 times. Direct egg transmission to ungulates is rare, and we suggest this is due to a transmission barrier caused by ungulate faecal avoidance. Our survey confirmed that ungulates are almost always definitive hosts, and we discuss the exceptional cases when they are not.