Hope Klug

The mismeasurement of sexual selection

Sexual selection can explain major micro‐ and macro‐evolutionary patterns. Much of current theory predicts that the strength of sexual selection (i) is driven by the relative abundance of males and females prepared to mate (i.e. the operational sex ratio, OSR) and (ii) can be generally estimated by calculating intra‐sexual variation in mating success (e.g. the opportunity for sexual selection, Is). Here, we demonstrate the problematic nature of these predictions. The OSR and Is only accurately predict sexual selection under a limited set of circumstances, and more specifically, only when mate monopolization is extremely strong. If mate monopolization is not strong, using OSR or Is as proxies or measures of sexual selection is expected to produce spurious results that lead to the false conclusion that sexual selection is strong when it is actually weak. These findings call into question the validity of empirical conclusions based on these measures of sexual selection.

When to Care for, Abandon, or Eat Your Offspring: The Evolution of Parental Care and Filial Cannibalism

Parental care and filial cannibalism (the consumption of one’s own offspring) co‐occur in many animals. While parental care typically increases offspring survival, filial cannibalism involves the killing of one’s young. Using an evolutionary ecology approach, we evaluate the importance of a range of factors on the evolution of parental care and filial cannibalism. Parental care, no care/total abandonment, and filial cannibalism evolved and often coexisted over a range of parameter space. While no single benefit was essential for the evolution of filial cannibalism, benefits associated with adult or offspring survival and/or reproduction facilitated the evolution of cannibalism. Our model highlights the plausibility of a range of alternative hypotheses. Specifically, the evolution of filial cannibalism was enhanced if (1) parents could selectively cannibalize lower‐quality offspring, (2) filial cannibalism increased egg maturation rate, (3) energetic benefits of eggs existed, or (4) cannibalism increased a parent’s reproductive rate (e.g., through mate attractiveness). Density‐dependent egg survivorship alone did not favor the evolution of cannibalism. However, when egg survival was density dependent, filial cannibalism invaded more often when the density dependence was relatively more intense. Our results suggest that population‐level resource competition potentially plays an important role in the evolution of both parental care and filial cannibalism.

The opportunity to be misled in studies of sexual selection

It is a challenge to measure sexual selection because both stochastic events (chance) and deterministic factors (selection) generate variation in individuals’ reproductive success. Most researchers realize that random events (‘noise’) make it difficult to detect a relationship between a trait and mating success (i.e. the presence of sexual selection). There is, however, less appreciation of the dangers that arise if stochastic events vary systematically. Systematic variation makes variance‐based approaches to measuring the role of selection problematic. This is why measuring the opportunity for sexual selection (Is and Imates) is so vulnerable to misinterpretation. Although Is does not measure actual sexual selection (because it includes stochastic variation in mating/fertilization success) it is often implicitly assumed that it will be correlated with the actual strength of sexual selection. The hidden assumption is that random noise is randomly distributed across populations, species or the sexes. Here we present a simple numerical example showing why this practice is worrisome. Specifically, we show that chance variation in mating success is higher when there are fewer potential mates per individual of the focal sex [i.e. when the operational sex ratio (OSR), is more biased]. This will lead to the OSR covarying with Is even when the strength of sexual selection is unaffected by the OSR. This can generate false confidence in identifying factors that determine variation in the strength of sexual selection. We emphasize that in nature, even when sexual selection is strong, chance variation in mating success is still inevitable because the number of mates per individual is a discrete number. We hope that our worked example will clarify a recent debate about how best to measure sexual selection.

LIFE HISTORY AND THE EVOLUTION OF PARENTAL CARE

Patterns of parental care are strikingly diverse in nature, and parental care is thought to have evolved repeatedly multiple times. Surprisingly, relatively little is known about the most general conditions that lead to the origin of parental care. Here, we use a theoretical approach to explore the basic life‐history conditions (i.e., stage‐specific mortality and maturation rates, reproductive rates) that are most likely to favor the evolution of some form of parental care from a state of no care. We focus on parental care of eggs and eggs and juveniles and consider varying magnitudes of the benefits of care. Our results suggest that parental care can evolve under a range of life‐history conditions, but in general will be most strongly favored when egg death rate in the absence of care is high, juvenile survival in the absence of care is low (for the scenario in which care extends into the juvenile stage), adult death rate is relatively high, egg maturation rate is low, and the duration of the juvenile stage is relatively short. Additionally, parental care has the potential to be favored at a broad range of adult reproductive rates. The relative importance of these life‐history conditions in favoring or limiting the evolution of care depends on the magnitude of the benefits of care, the relationship between initial egg allocation and subsequent offspring survival, and whether care extends into the juvenile stage. The results of our model provide a general set of predictions regarding when we would expect parental care to evolve from a state of no care, and in conjunction with other work on the topic, will enhance our understanding of the evolutionary dynamics of parental care and facilitate comparative analyses.

Who to include in measures of sexual selection is no trivial matter

In many animals acquiring limited reproductive opportunities involves competition for resources, mates and opposite-sex gametes. There is ambiguity in which competitive steps are included in measures of sexual selection: individuals who fail to obtain resources necessary for reproduction are often excluded. We illustrate the implications of variation in who is included in measures of selection. We quantified selection on male length and the opportunity for selection associated with nest acquisition, mate acquisition, and fertility of mates at two levels of density and two levels of nest availability in the sand goby. Both measures varied significantly across the three episodes of selection. Nest and mate acquisition contributed substantially to the overall opportunity for selection and selection on male size. Focusing only on males with nests led to lower estimates of selection. The effects of density and nest availability depended on the selective episodes considered. While there is nothing wrong with focusing on particular episodes of interest, inconsistency in who is included in measures of sexual selection across studies will make it difficult to answer broad research questions.

What are the benefits of parental care? The importance of parental effects on developmental rate

The evolution of parental care is beneficial if it facilitates offspring performance traits that are ultimately tied to offspring fitness. While this may seem self-evident, the benefits of parental care have received relatively little theoretical exploration. Here, we develop a theoretical model that elucidates how parental care can affect offspring performance and which aspects of offspring performance (e.g., survival, development) are likely to be influenced by care. We begin by summarizing four general types of parental care benefits. Care can be beneficial if parents (1) increase offspring survival during the stage in which parents and offspring are associated, (2) improve offspring quality in a way that leads to increased offspring survival and/or reproduction in the future when parents are no longer associated with offspring, and/or (3) directly increase offspring reproductive success when parents and offspring remain associated into adulthood. We additionally suggest that parental control over offspring developmental rate might represent a substantial, yet underappreciated, benefit of care. We hypothesize that parents adjust the amount of time offspring spend in life-history stages in response to expected offspring mortality, which in turn might increase overall offspring survival, and ultimately, fitness of parents and offspring. Using a theoretical evolutionary framework, we show that parental control over offspring developmental rate can represent a significant, or even the sole, benefit of care. Considering this benefit influences our general understanding of the evolution of care, as parental control over offspring developmental rate can increase the range of life-history conditions (e.g., egg and juvenile mortalities) under which care can evolve.

The origin of parental care in relation to male and female life history

The evolution of maternal, paternal, and bi-parental care has been the focus of a great deal of research. Males and females vary in basic life-history characteristics (e.g., stage-specific mortality, maturation) in ways that are unrelated to parental investment. Surprisingly, few studies have examined the effect of this variation in male and female life history on the evolution of care. Here, we use a theoretical approach to determine the sex-specific life-history characteristics that give rise to the origin of paternal, maternal, or bi-parental care from an ancestral state of no care. Females initially invest more into each egg than males. Despite this inherent difference between the sexes, paternal, maternal, and bi-parental care are equally likely when males and females are otherwise similar. Thus, sex differences in initial zygotic investment do not explain the origin of one pattern of care over another. However, sex differences in adult mortality, egg maturation rate, and juvenile survival affect the pattern of care that will be most likely to evolve. Maternal care is more likely if female adult mortality is high, whereas paternal care is more likely if male adult mortality is high. These findings suggest that basic life-history differences between the sexes can alone explain the origin of maternal, paternal, and bi-parental care. As a result, the influence of life-history characteristics should be considered as a baseline scenario in studies examining the origin of care.

The net effects of guarding on egg survivorship in the flagfish, Jordanella floridae

We investigated the effects of male nest guarding on egg survival in the flagfish, a species in which paternal care is thought to be relatively recently evolved. Thus, we characterized the fitness consequences of a major component of paternal care when secondary adaptations to care are likely to be minimal. The effects of guarding under three predation regimes were examined by exposing eggs to treatments in which no predators, conspecific females, and conspecific females and the egg predator Gambusia affinis were present. These were crossed with the presence and absence of parental males. We expected that guarding would result in an increase in egg survival in the presence of egg predators, but considered that in their absence the benefit might be decreased or absent, as a result of filial cannibalism. We also examined effects on egg survivorship stemming from filial cannibalism and egg-directed components of care (i.e. cleaning and fanning); the effects of these behaviours were examined through treatments in which males had full access to eggs (i.e. complete care), males were separated from their eggs by a screen (i.e. egg fanning and no cannibalism), and males were absent (i.e. no care and no cannibalism). In accordance with our expectations, guarding increased egg survivorship in the presence of females and Gambusia. However, egg survivorship when males were alone with eggs was low. Indeed, significantly more eggs were eaten than became diseased, suggesting that males cannibalize healthy eggs. Neither fanning nor cleaning resulted in an increase in egg survivorship. Thus, in flagfish, there may be costs of care when predators are absent. We discuss our findings in relation to sexual selection and the early evolution of parental care.

Sex differences in life history drive evolutionary transitions among maternal, paternal, and bi-parental care.

Evolutionary transitions among maternal, paternal, and bi-parental care have been common in many animal groups. We use a mathematical model to examine the effect of male and female life-history characteristics (stage-specific maturation and mortality) on evolutionary transitions among maternal, paternal, and bi-parental care. When males and females are relatively similar – that is, when females initially invest relatively little into eggs and both sexes have similar mortality and maturation – transitions among different patterns of care are unlikely to be strongly favored. As males and females become more different, transitions are more likely. If females initially invest heavily into eggs and this reduces their expected future reproductive success, transitions to increased maternal care (paternal → maternal, paternal → bi-parental, bi-parental → maternal) are favored. This effect of anisogamy (i.e., the fact that females initially invest more into each individual zygote than males) might help explain the predominance of maternal care in nature and differs from previous work that found no effect of anisogamy on the origin of different sex-specific patterns of care from an ancestral state of no care. When male mortality is high or male egg maturation rate is low, males have reduced future reproductive potential and transitions to increased paternal care (maternal → paternal, bi-parental → paternal, maternal → bi-parental) are favored. Offspring need (i.e., low offspring survival in the absence of care) also plays a role in transitions to paternal care. In general, basic life-history differences between the sexes can drive evolutionary transitions among different sex-specific patterns of care. The finding that simple life-history differences can alone lead to transitions among maternal and paternal care suggests that the effect of inter-sexual life-history differences should be considered as a baseline scenario when attempting to understand how other factors (mate availability, sex differences in the costs of competing for mates) influence the evolution of parental care.

Should you eat your offspring before someone else does? Effect of an egg predator on filial cannibalism in the sand goby

Costs and benefits of parental care are expected to affect filial cannibalism. One factor that increases the costs and decreases the benefits of care is the presence of egg predators. In general, the effect of egg predators on filial cannibalism is unknown. Here, we examine the effect of an egg predator on filial cannibalism in the sand goby. Males caring for eggs were exposed to three treatments: no egg predator, visual cues from an egg predator, and chemical and visual cues from an egg predator. We hypothesized that the perceived benefits of providing care in the presence of an egg predator would be relatively low, and we expected filial cannibalism to increase in the presence of the egg predator, especially when both chemical and visual predator cues were present, as this might represent a greater threat. When both visual and chemical predator cues were present, whole-clutch cannibalism increased. In addition, larger males and males in poorer condition showed less whole-clutch cannibalism than smaller males or males in better condition. There was no effect of egg predator on partial-clutch cannibalism. However, males that engaged in partial-clutch cannibalism ate more of their eggs when the eggs were spawned by a female in relatively good condition, but a smaller proportion and number of eggs when only a single female spawned. In general, our findings suggest that male sand gobies are sensitive to the costs and benefits of care and are more likely to terminate care when the expected benefits are relatively low.