Jussi Lehtonen

Negative Frequency-Dependent Selection of Sexually Antagonistic Alleles in Myodes glareolus

Selection of rare-male types in a population can maintain genetic variation that benefits one sex but harms the other. Sexually antagonistic genetic variation, where optimal values of traits are sex-dependent, is known to slow the loss of genetic variance associated with directional selection on fitness-related traits. However, sexual antagonism alone is not sufficient to maintain variation indefinitely. Selection of rare forms within the sexes can help to conserve genotypic diversity. We combined theoretical models and a field experiment with Myodes glareolus to show that negative frequency-dependent selection on male dominance maintains variation in sexually antagonistic alleles. In our experiment, high-dominance male bank voles were found to have low-fecundity sisters, and vice versa. These results show that investigations of sexually antagonistic traits should take into account the effects of social interactions on the interplay between ecology and evolution, and that investigations of genetic variation should not be conducted solely under laboratory conditions.

Positive feedback and alternative stable states in inbreeding, cooperation, sex roles and other evolutionary processes

A large proportion of studies in systems science focus on processes involving a mixture of positive and negative feedbacks, which are also common themes in evolutionary ecology. Examples of negative feedback are density dependence (population regulation) and frequency-dependent selection (polymorphisms). Positive feedback, in turn, plays a role in Fisherian ‘runaway’ sexual selection, the evolution of cooperation, selfing and inbreeding tolerance under purging of deleterious alleles, and the evolution of sex differences in parental care. All these examples feature self-reinforcing processes where the increase in the value of a trait selects for further increases, sometimes via a coevolutionary feedback loop with another trait. Positive feedback often leads to alternative stable states (evolutionary endpoints), making the interpretation of evolutionary predictions challenging. Here, we discuss conceptual issues such as the relationship between self-reinforcing selection and disruptive selection. We also present an extension of a previous model on parental care, focusing on the relationship between the operational sex ratio and sexual selection, and the influence of this relationship on the evolution of biparental or uniparental care.

Two roads to two sexes: unifying gamete competition and gamete limitation in a single model of anisogamy evolution

Recent studies have revealed the importance of self-consistency in evolutionary models, particularly in the context of male–female interactions. This has been largely ignored in models of the ancestral divergence of the sexes, i.e., the evolution of anisogamy. Here, we model the evolution of anisogamy in a Fisher-consistent context, explicitly taking into account the number of interacting individuals in a typical reproductive group. We reveal an interaction between the number of adult individuals in the local mating group and the selection pressures responsible for the divergence of the sexes. The same underlying model can produce anisogamy in two different ways. Gamete competition can lead to anisogamy when it is relatively easy for gametes to find each other, but when this is more difficult and gamete competition is absent, gamete limitation can provide another route for anisogamy to evolve. In line with earlier models, organismal complexity favors anisogamy. We argue that the early contributions of Kalmus and Scudo, largely dismissed as group selectionist, are valid under certain conditions. Linking their work with the contributions of Parker helps to explain why precisely males keep producing more sperm than can ever lead to offspring: sperm could evolve to provision zygotes but this brings little profit for the effort required, because sperm would have to be equipped with provisioning ability before it is known which sperm will make it to the fertilization stage. This insight creates a logical link between paternal care under uncertain paternity (where again investment is selected against when some investment never brings about genetic benefits) and gamete size evolution.

Safety in numbers: the dilution effect and other drivers of group life in the face of danger

Animals can congregate in groups for many reasons, from reproductive assurance to improved foraging or predation efficiency, to avoiding themselves becoming the target of predation by other animals. It is the last category that is the focus of this review: group living as protection from predation. The drivers of group life in the face of danger are at the same time diverse and interlinked, with much potential for confusion between concepts. Here we review these concepts, using the dilution effect as a starting point. We construct a mathematical model that allows us to examine various features of the dilution effect and their connection to ecology. We also show the importance of including a time scale when modelling the dilution effect and how this translates into more realistic estimation of the fitness consequences of a diluted predation risk. The central role of the dilution effect in creating safety in numbers is underlined by showing how it may affect life-history evolution and result in the emergence of gregarious life-history strategies, even among sessile organisms limited in their abilities to exhibit behavioural responses to predation. Finally, we review the other central processes underpinning group protection from predation: the satiation effect, selfish herding, the confusion effect and group vigilance.

What do isogamous organisms teach us about sex and the two sexes

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 ancestors. Furthermore, because maleness is synonymous with the production of small gametes, an explanation for the initial origin of males and females is synonymous with understanding the transition from isogamy to anisogamy. As we show here, this transition may also be crucial for understanding why sex itself remains common even in taxa with high costs of male production (the twofold cost of sex). The transition to anisogamy implies the origin of male and female sexes, kickstarts the subsequent evolution of sex roles, and has a major impact on the costliness of sexual reproduction. Finally, we combine some of the consequences of isogamy and anisogamy in a thought experiment on the maintenance of sexual reproduction. We ask what happens if there is a less than twofold benefit to sex (not an unlikely scenario as large short-term benefits have proved difficult to find), and argue that this could lead to a situation where lineages that evolve anisogamy—and thus the highest costs of sex—end up being associated with constraints that make invasion by asexual reproduction unlikely (the ‘anisogamy gateway’ hypothesis). This article is part of the themed issue ‘Weird sex: the underappreciated diversity of sexual reproduction’.

Why anisogamy drives ancestral sex roles

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 females. However, this view has recently been challenged, and a formal validation of the link between anisogamy and sex roles has been lacking. Here, we develop mathematical models that validate the intuition of Darwin and Bateman, showing that there is a very simple and general reason why unequal gamete numbers result in unequal investment in sexually competitive traits. This asymmetry does not require multiple mating by either sex, and covers traits such as mate searching, where the male bias has been difficult to explain. Furthermore, our models show males and females are predicted to diverge more strongly when the fertilization probability of each female gamete is high. Sex roles thus ultimately trace back to anisogamy and the resulting consequences for the fertilization process.

Gamete evolution and sperm numbers: sperm competition versus sperm limitation

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. We show quite generally for the intensity model (where N males compete for each set of eggs) that however severe the degree of SL, if there is at least one competitor for fertilization (N − 1 ≥ 1), the marginal gains through SC exceed those for SL, provided that the relationship between the probability of fertilization (F) and increasing sperm numbers (x) is a concave function. In the risk model, as fertility F increases from 0 to 1.0, the threshold SC risk (the probability q that two males compete for fertilization) for SC to be the dominant force drops from 1.0 to 0. The gamete competition and gamete limitation theories for the evolution of anisogamy rely on very similar considerations: our results imply that gamete limitation could dominate only if ancestral reproduction took place in highly isolated, small spawning groups.

Why inclusive fitness can make it adaptive to produce less fit extra-pair offspring

Social monogamy predominates in avian breeding systems, but most socially monogamous species engage in promiscuous extra-pair copulations (EPCs). The reasons behind this remain debated, and recent empirical work has uncovered patterns that do not seem to fit existing hypotheses. In particular, some results seem to contradict the inbreeding avoidance hypothesis: females can prefer extra-pair partners that are more closely related to them than their social partners, and extra-pair young can have lower fitness than within-pair young. Motivated by these studies, we show that such results can become explicable when an asymmetry in inbreeding tolerance between monogamy and polygamy is extended to species that combine both strategies within a single reproductive season. Under fairly general conditions, it can be adaptive for a female to choose an unrelated social partner, but inbreed with an extra-pair partner. Inbreeding depression is compensated for by inclusive fitness benefits, which are only fully realized in EPCs. We also show that if a female has already formed a suboptimal social bond, there are scenarios where it is beneficial to engage in EPCs with less related males, and others where EPCs with more related males increase her inclusive fitness. This has implications for detecting general relatedness or fitness trends when averaged over several species.

Gamete competition, gamete limitation, and the evolution of the two sexes

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 isogamous, meaning that only one gamete size was produced. The question of the evolutionary origin of males and females is then synonymous to asking what evolutionary pressures caused gamete sizes to diverge. Studying the ancestral evolutionary divergence of males and females relies largely on mathematical modelling. Here, we review two classes of models explaining the evolutionary origin of males and females: gamete competition and gamete limitation. These seemingly alternative explanations are not mutually exclusive, but two aspects of a single evolutionary process. Once evolved, anisogamy and the two sexes are evolutionarily very stable. This explains the maintenance of anisogamy in organisms with internal fertilization, which can cause large decreases in both gamete competition and gamete limitation. The ancestral divergence and maintenance of gamete sizes subsequently led to many other differences we now observe between the two sexes, sowing the seeds for what we have become.

Generation time, life history and the substitution rate of neutral mutations

Our understanding of molecular evolution is hampered by a lack of quantitative predictions about how life-history (LH) traits should correlate with substitution rates. Comparative studies have shown that neutral substitution rates vary substantially between species, and evidence shows that much of this diversity is associated with variation in LH traits. However, while these studies often agree, some unexplained and contradictory results have emerged. Explaining these results is difficult without a clear theoretical understanding of the problem. In this study, we derive predictions for the relationships between LH traits and substitution rates in iteroparous species by using demographic theory to relate commonly measured life-history traits to genetic generation time, and by implication to neutral substitution rates. This provides some surprisingly simple explanations for otherwise confusing patterns, such as the association between fecundity and substitution rates. The same framework can be applied to more complex life histories if full life-tables are available.