Geoff A. Parker

University of Liverpool | UoL · Evolution, Ecology and Behaviour

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 d...

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...

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 evoluti...

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 c...

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 Holothur...

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, a...

We currently classify sexual selection into pre- and post-copulatory components. In fact, pre-copulatory sexual selection (as envisaged by Darwin) represents the final stages of a cascade of events in the evolution of sexual strategy (the ‘sexual cascade’), each stage arising as a consequence of the stage before. The cascade begins with the evoluti...

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...

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...

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 guardin...

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...

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...

Parasitic worms with complex life cycles have several developmental stages, with each stage creating opportunities to infect additional host species. Using a dataset 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 dive...

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...

In recent years, the field of sexual selection has exploded, with advances in theoretical and empirical research complementing each other in exciting ways. This perspective piece is the product of a ''stock-taking'' workshop on sexual selection and sexual conflict. Our aim is to identify and deliberate on outstanding questions and to stimulate disc...

In recent years, the field of sexual selection has exploded, with advances in theoretical and empirical research complementing each other in exciting ways. This perspective piece is the product of a “stock-taking” workshop on sexual selection and conflict. Our aim is to identify and deliberate on outstanding questions and to stimulate discussion ra...

Transition from isogamy to anisogamy, hence males and females, leads to sexual selection, sexual conflict, sexual dimorphism, and sex roles. Gamete dynamics theory links biophysics of gamete limitation, gamete competition, and resource requirements for zygote survival and assumes broadcast spawning. It makes testable predic- tions, but most compara...

The field of sexual selection has burgeoned with research into trait evolution in the context of ecology, sociality, phylogeny, natural selection, and sexual conflict. This paper is the product of a “stock-taking” workshop; our aim is to stimulate discussion, not to provide an exhaustive review. We identify outstanding questions organized into four...

The field of sexual selection has burgeoned with research into trait evolution in the context of ecology, sociality, phylogeny, natural selection, and sexual conflict. This paper is the product of a “stock-taking” workshop; our aim is to stimulate discussion, not to provide an exhaustive review. We identify outstanding questions organized into four...

On the occasion of the XIIIth International Symposium on Spermatology held from 9 to 13 May 2018 in Stockholm (Sweden), participants (guest speakers and audience) collectively felt the need to make a public statement on the general issue of male reproductive health. Our intention is to raise awareness of what we believe is a neglected area of resea...

Reproductive studies of an intertidal free-spawning population of Chiton articulatus (Mollusca: Polyplacophora) from Puerto Angel, Oaxaca, Mexico were undertaken during 2011. We used gonad histology and gonadal indices to assess the relative gonad expenditure of the sexes (RGES) and other reproductive traits, accounting for individual and seasonal...

Sedentary broadcast-spawning marine invertebrates, which release both eggs and sperm into the water for fertilization, are of special interest for sexual selection studies. They provide unique insight into the early stages of the evolutionary succession leading to the often-intense operation of both pre- and post-mating sexual selection in mobile g...

Isogamy is a reproductive system where all gametes are morphologically similar, especially in terms of size. Its importance goes beyond specific cases: to this day non-anisogamous systems are common outside of multicellular animals and plants, they can be found in all eukaryotic super-groups, and anisogamous organisms appear to have isogamous ances...

There is a clear tendency in nature for males to compete more strongly for fertilizations than females, yet the ultimate reasons for this are still unclear. Many researchers - dating back to Darwin and Bateman - have argued that the difference is ultimately driven by the fact that males (by definition) produce smaller and more numerous gametes than...

Evolutionary theory for expenditure on gonads attracted little attention until studies in the past 3–4 decades of allocation to male and female function in hermaphrodites, and of relative testes size (RTS) in animals with separate sexes. RTS appears to have varied enormously over evolutionary time, from extremely high (over 40%) in some broadcast s...

Modern sexual selection theory, developed from Darwin’s original intuition, is a cornerstone of evolutionary theory and represents the most parsimonious and robust explanation for a bewildering array of evolutionary patterns and diversity. Here we first outline the principles of modern sexual selection theory and discuss their heuristic value. Seco...

We review how trophically transmitted helminths adapt to the special problems associated with successive hosts in complex cycles. In intermediate hosts, larvae typically show growth arrest at larval maturity (GALM). Theoretical models indicate that optimization of size at GALM requires larval mortality rate to increase with time between infection a...

Links between parasites and food webs are evolutionarily ancient but dynamic: life history theory provides insights into helminth complex life cycle origins. Most adult helminths benefit by sexual reproduction in vertebrates, often high up food chains, but direct infection is commonly constrained by a trophic vacuum between free-living propagules a...

Parasitic worms (helminths) frequently have complex life cycles in which they are transmitted trophically between two or more successive hosts. Sexual reproduction often takes place in high trophic-level (TL) vertebrates, where parasites can grow to large sizes with high fecundity. Direct infection of high TL hosts, while advantageous, may be unach...

Males and females are a fundamental aspect of human reproduction, yet procreation is perfectly possible without this division into two sexes. Biologically, males are defined as the sex that produces the smaller gametes (e.g. sperm), implying that the male and female sexes only exist in species with gamete dimorphism (anisogamy). Our ancestors were...

Both gamete competition and gamete limitation can generate anisogamy from ancestral isogamy, and both sperm competition (SC) and sperm limitation (SL) can increase sperm numbers. Here, we compare the marginal benefits due to these two components at any given population level of sperm production using the risk and intensity models in sperm economics...

After brief historic overviews of sexual selection and sexual conflict, I argue that pre-ejaculatory sexual selection (the form of sexual selection discussed by Darwin) arose at a late stage in an inevitable succession of transitions flowing from the early evolution of syngamy to the evolution of copulation and sex roles. If certain conditions were...

Many birds show biparental incubation patterns in which male and female parents alternate their incubation bouts. We constructed prospective sealed bid (rather than negotiation) models of optimal (both cooperative and ESS) incubation bout lengths for each sex (‘the incubation game’) to examine whether the asymmetry in incubation efficiency can gene...

We give a historic overview and critical perspective of polyandry in the context of sexual selection. Early approaches tended to obfuscate the fact that the total matings (copulations) by the two sexes is equal, neglecting female interests and that females often mate with (or receive ejaculates from) more than one male (polyandry). In recent years,...

Reproductive males face a trade-off between expenditure on precopulatory male-male competition-increasing the number of females that they secure as mates-and sperm competition-increasing their fertilization success with those females. Previous sperm allocation models have focused on scramble competition in which males compete by searching for mates...

Abstract Organisms with complex life cycles occupy distinct niches as larvae and adults. One presumed advantage of this is the ability to exploit different resources successively throughout ontogeny. Various taxa, however, have evolved nonfeeding, nongrowing adult stages. We show theoretically that this counterintuitive no-growth strategy is favore...

Switching from one host to the next is a critical life-history transition in parasites with complex life cycles. Growth and mortality rates are thought to influence the optimal time and size at transmission, but these rates are difficult to measure in parasites. The parasite life cycle, in particular the trophic link along which transmission occurs...

INTRODUCTION. It is generally assumed (e.g. Maynard Smith, 1978; 1982) that ancestrally, gametes were small and isogamous (monomorphic). The evolution of anisogamy (gamete dimorphism) is a crucial transition in evolution (Maynard Smith and Szathmáry, 1995): it represents the evolution of the two sexes, males and females. Following Parker et al. (19...

Spermatozoa are amongst the most variable cells, and three factors are thought to account for this variation in design: fertilization mode, phylogeny, and postcopulatory sexual selection. In addition, it has long been assumed that a tradeoff exists between sperm size and number, and although postcopulatory sexual selection affects both traits, empi...

Arising from M. A. Nowak, C. E. Tarnita & E. O. Wilson 466, 1057-1062 (2010); Nowak et al. reply. Nowak et al. argue that inclusive fitness theory has been of little value in explaining the natural world, and that it has led to negligible progress in explaining the evolution of eusociality. However, we believe that their arguments are based upon a...

But I now see that the whole problem is so intricate that it is safer to leave its solution for the future. Darwin (1874) on the evolution of the unity sex ratio; later solved by Fisher (1930) A vital part of science is the compulsion to ask questions, even if, like Darwin, we cannot always find an answer. I admit to being surprised, almost offende...

Sperm competition was identified in 1970 as a pervasive selective force in post-copulatory sexual selection that occurs when the ejaculates of different males compete to fertilise a given set of ova. Since then, sperm competition has been much studied both empirically and theoretically. Because sperm competition often favours large ejaculates, an i...

We examine models for evolution of sperm size (i.e. mass m) and number (s) under three mechanisms of sperm competition at low 'risk' levels: (i) raffle with no constraint on space available for competing sperm, (ii) direct displacement mainly by seminal fluid, and (iii) direct displacement mainly by sperm mass. Increasing sperm mass increases a spe...

Life-history theory predicts an optimal offspring size, irrespective of reproductive effort; however, in some species offspring size correlates positively with maternal size. We examine hypotheses for why this latter situation should occur in the whelk Buccinum undatum. The trade-offs between aspects of reproduction in whelks are complicated due to...

Sperm competition is the competition between the ejaculates of different males for the fertilization of a given set of ova. Charles Darwin (1871) proposed sexual selection as a process that operates on variation in male ability to compete with other males for access to reproductive opportunities, and which promotes traits that confer an advantage i...

In the complex life cycles of helminths, life in intermediate hosts poses special problems not covered by standard life history strategy theory. While under selection to reduce mortality and to increase growth, there is the additional problem of transmission between hosts. This review attempts to harmonise classical knowledge of the overall life cy...

In complex life cycles, larval helminths typically migrate from the gut to exploit the tissues of their intermediate hosts. Yet the definitive host's gut is overwhelmingly the most favoured site for adult helminths to release eggs. Vertebrate nematodes with one-host cycles commonly migrate to a site in the host away from the gut before returning to...

Larval helminths in intermediate hosts often stop growing long before their growth is limited by host resources, and do not grow at all in paratenic hosts. We develop our model [Ball, M.A., Parker, G.A., Chubb, J.C., 2008. The evolution of complex life cycles when parasite mortality is size- or time-dependent. J. Theor. Biol. 253, 202-214] for opti...

Many trophically transmitted parasites have complex life cycles: they pass through at least one intermediate host before reproducing in their final host. Despite their economic and theoretical importance, the evolution of such cycles has rarely been investigated. Here, combining a novel modeling approach with experimental data, we show for the firs...

SYNOPSISField data on male reproductive searching activity in Scatophaga is compared with that for non-reproductive behaviour. The effects of high and low male density are investigated and the sequential organisation of the search pattern is analyse and discussed.

We investigate evolution of two categories of adaptive host manipulation by trophically transmitted helminths: (1) predation suppression decreases the host's mortality before the helminth is capable of establishing in its next host; (2) predation enhancement increases the existing host's mortality after it can establish in its next host. If all par...

In complex cycles, helminth larvae in their intermediate hosts typically grow to a fixed size. We define this cessation of growth before transmission to the next host as growth arrest at larval maturity (GALM). Where the larval parasite controls its own growth in the intermediate host, in order that growth eventually arrests, some form of size- or...

We examine the risk model in sperm competition games for cases where female fertility increases significantly with sperm numbers (sperm limitation). Without sperm competition, sperm allocation increases with sperm limitation. We define 'average risk' as the probability q that females in the population mate twice, and 'perceived risk' as the informa...

Question: Can intrasexual selection on male size and natural selection on female size in the shell-brooding cichlid Lamprologus callipterus explain the greatest male/female sexual size dimorphism (SSD) reported to date among animals? Mathematical methods: (1) Mortality model to predict male and female body sizes. (2) Gain rate maximization and (3)...

Although most (>90%) species of birds have biparental care, little is known about the consequences of such care for offspring behaviour and fitness-related traits. We examined the effect of biparental care on chick growth and begging behaviour in zebra finches, by comparing biparental broods with uniparental broods in which the male parent was remo...

Sexual conflict is a conflict between the evolutionary interests of individuals of the two sexes. The sexes can have different trait optima but this need not imply conflict if their optima can be attained simultaneously. Conflict requires an interaction between males and females (e.g. mating or parental care), such that the optimal outcomes for eac...

In parasites with a complex life cycle, the fitness of an individual depends on its probability of reaching the final host and on its fecundity. Because larval growth in intermediate hosts may affect both transmission and adult size, selection should optimize growth patterns that are conditional on the presence and number of conspecific competitors...

It is suggested that sperm competition (competition between the sperm from two or more males over the fertilization of ova) may account for the fact that sperm are so small and so numerous. In the entire absence of sperm competition, selection may favour an increase in sperm size so that the sperm contributes nutriment to the subsequent viability a...

We explored behavioural adjustments made by parent house sparrows, Passer domesticus, when the nutritional condition of their dependent nestlings was improved experimentally. Male parents responded to artificially supplemented broods by increasing food deliveries, whereas female parents continued matching the already high rate of control females. T...

There are various ways to estimate ejaculate expenditure. Ejaculate size or sperm number (s) is an absolute number of units of ejaculate. Relative ejaculate expenditure (E) is the expenditure on the ejaculate as the proportion of the total expenditure on all aspects of the mating, including finding and acquiring a female, and so on. Relative testis...

Sperm competition is a pervasive selective force in evolution, shaping reproductive anatomy, physiology and behaviour. Here, we present comparative evidence that varying sperm competition levels account for variation in the male reproductive anatomy of rodents, the largest and most diverse mammalian order. We focus on the sperm-producing testes and...

This study sampled sperm from wild Atlantic salmon to explore relationships between sperm form and function. Detailed measurements of sperm morphometry (head, flagellum and total length) and sperm activity (longevity and % motility) were made from 24 reproductively active males (13 anadromous and 11 mature parr) on two occasions post-stripping. The...

We describe six polymorphic, trinucleotide microsatellite loci that were isolated from the yellow dung fly Scathophaga stercoraria (Diptera: Scathophagidae), a model system for examining the mechanisms behind sperm competition in species with internal fertilization. These microsatellites yielded between 3 and 11 alleles per locus in a sample of 20–...

Trivers proposed that, if parental care by both sexes is advantageous, males should practice a "mixed" strategy of seeking extrapair copulations, while restricting their parental investment to offspring of social mates. We explore circumstances under which males should limit their parental care in the predicted manner. We find that Trivers's "mixed...

The pattern of parental investment (PI) seen in nature is a product of the simultaneous resolution of conflicts of interest between the members of a family. How these conflicts are resolved depends upon the mating system, the genetic mechanism, on whether extra PI affects current or future offspring, and the behavioural mechanisms underlying supply...

Sperm competition occurs when sperm from more than one male compete for fertilizations. This form of post-copulatory sexual selection is recognized as a significant and widespread force in the evolution of male reproductive biology and as a key determinant of differential male reproductive success. Despite its importance, however, detailed mechanis...

The fundamental question of how complex life cycles--where there is typically more than one host-evolve in host--parasite systems remains largely unexplored. We suggest that complex cycles in helminths without penetrative infective stages evolve by two essentially different processes, depending on where in the cycle a new host is inserted. In 'upwa...

We analyse a co-evolutionary sexual conflict game, in which males compete for fertilizations (sperm competition) and females operate sperm selection against unfavourable ejaculates (cryptic female choice). For simplicity, each female mates with two males per reproductive event, and the competing ejaculates are of two types, favourable (having high...

We consider optimal growth of larval stages in complex parasite life cycles where there is no constraint because of host immune responses. Our model predicts an individual's asymptotic size in its intermediate host, with and without competition from conspecific larvae. We match observed variations in larval growth patterns in pseudophyllid cestodes...

Correction for ‘The evolution of anisogamy: a game-theoretic approach’ by M. G. Bulmer and G. A. Parker (Proc. R. Soc. Lond. B 269 , 2381–2388. (doi: [10.1098/rspb.2002.2161][1])). On page 2383, below equation (2.8), the first sentence of the new paragraph should read: [1]: /lookup/doi/10.1098/rspb.2002.2161

Recently refined evolutionary theories propose that sexual selection and reproductive conflict could be drivers of speciation. Male and female reproductive optima invariably differ because the potential reproductive rate of males almost always exceeds that of females: females are selected to maximize mate 'quality', while males can increase fitness...

A popular theory has proposed that anisogamy originated through disruptive selection acting on an ancestral isogamous population, though recent work has emphasized the importance of other factors in its evolution. We re-examine the disruptive selection theory, starting from an isogamous population with two mating types and taking into account the f...

Mammal life history traits relating to growth and reproduction are extremely diverse. Sibling rivalry may contribute to selection pressures influencing this diversity, because individuals that are relatively large at birth typically have an advantage in competition for milk. However, selection for increased growth rate is likely to be constrained b...

There is burgeoning interest in the idea that conspicuous begging displays, when parents are provisioning dependent young, advertise offspring need honestly to parents. Many empirical studies claim to support the theory of honest signalling of need, where parents control resource allocation. The evidence, however, also fits the predictions of recen...

We explored the responses of monogamous house sparrow parents to deviations in their mates' contributions to nestling provisioning. Following 1-2 days of baseline measurement of parental food delivery rates, we applied small lead fishing weights to the tail feathers of either male or female parents. Weighting had much greater immediate impact on ma...

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Sperm are produced in astronomical numbers compared with eggs, and there is good evidence that sperm competition is the force behind the evolution of many tiny sperm. However, sperm production inevitably has costs. Recent research shows that male ejaculate expenditure is dynamic in both time and space, and that males are sensitive to risks of sperm...

Parental care is often costly(1); hence, in sexually reproducing species where both male and female parents rear their offspring (biparental care), sexual conflict over parental investment can arise(2). Such conflict occurs because each care-giver would benefit from withholding parental investment for use with another partner, leading to a reductio...

Relationships between spermatozoal design and swimming behaviour were investigated using the significant natural variance in sperm traits in Atlantic salmon Salmo salar. In vitro motility and fertilization experiments were conducted with 86 Atlantic salmon to measure sperm form and function under natural fertilization conditions. Spermatozoal trait...