Life history and the evolutionary loss of parental care.

Parental care has been gained and lost evolutionarily multiple times. While many studies have focused on the origin of care, few have explored the evolutionary loss of care. Understanding the loss of parental care is important as the conditions that favour its loss will not necessarily be the opposite of those that favour the evolution of care. Evolutionary hysteresis (the case in which evolution depends on the history of a system) could create a situation in which it is relatively challenging to lose care once it has evolved. Here, using a mathematical approach, we explore the evolutionary loss of parental care in relation to basic life-history conditions. Our results suggest that parental care is most likely to be lost when egg and adult death rates are low, eggs mature quickly, and the level of care provided is high. We also predict evolutionary hysteresis with respect to egg maturation rate: as egg maturation rate decreases, it becomes increasingly more costly to lose care than to gain it. This suggests that once care is present, it will be particularly challenging for it to be lost if eggs develop slowly.

Life history, mating dynamics and the origin of parental care.

Parental care, mating dynamics and life history co-evolve. Understanding the diversity of reproductive patterns found in nature is a major focus of evolutionary ecology research. Previous research suggests that the origin of parental care of eggs will be favoured when egg and adult death rates and juvenile survival are relatively high. However, the previous research that explored the link between care and life history did not account for among-species variation in mating dynamics. As mating dynamics are generally expected to influence care, we explore, theoretically, the life-history conditions (stage-specific rates of maturation and survival) that favour parental care across three mating scenarios: reproductive rate (1) is unaffected by males (assuming that some males are present), (2) increases as male abundance increases or (3) decreases as male abundance increases. Across scenarios, all forms of care were most strongly favoured when egg and adult death rates, juvenile survival and female egg maturation rates were relatively high. When reproductive rate was unaffected by male abundance or increased as male abundance increased, as we might expect in systems in which females are mate-limited, all forms of care were most strongly favoured when male egg maturation rate (i.e. the rate at which male eggs develop, mature and hatch) was moderate or high. When greater male abundance inhibited reproduction, which might occur in systems with intense male-male competition, all forms of care were most strongly favoured when male egg maturation rate was low-to-moderate. These results suggest that life history affects the evolution of parental care, and sex-specific life history can interact with mating dynamics to influence the origin of care.

Coevolution influences the evolution of filial cannibalism, offspring abandonment and parental care.

Understanding evolutionary patterns of parental investment and care has been a long-standing focus in studies of evolutionary and behavioural ecology. Indeed, patterns of investment and care are highly diverse, and fully understanding such diversity has been challenging. Recently, several studies have highlighted the need to consider coevolutionary dynamics in studies of parental care, as parental care is likely to co-occur and co-originate with a range of other traits. Two traits that commonly co-occur with parental care are offspring abandonment (the termination of parental investment prior to full independence in offspring) and filial cannibalism (the consumption of one's offspring). Here, we use a mathematical framework to explore how co-occurrence and coevolution among care, abandonment and cannibalism can influence the life-history conditions under which care is expected to evolve. Our results suggest that in some cases, the evolution of parental care can be inhibited by offspring abandonment and filial cannibalism. In other cases, abandonment and filial cannibalism that benefits parents can promote the evolution of parental care. It is particularly interesting that behaviours that seem so contrary to care-that is, eating or abandoning one's young-can in some cases broaden the conditions under which care can evolve. In general, our findings highlight that considering co-occurrence and coevolutionary dynamics between two or more traits is essential to understanding the evolution of trait diversity.

Sexual selection and life history interact to influence the evolution of paternal care.

Parental care is essential to offspring survival in many species. Understanding why males of some species provide care, whereas others do not, has received substantial attention. Previous research has found that sexual selection can favor paternal care, yet we still do not fully understand why sexual selection favors male care in some species but not others. It is also unclear when paternal care versus other preferred male trait(s) will be favored by sexual selection. We hypothesize that sexual selection can interact with basic life history to influence the conditions under which paternal care and/or another preferred male trait will be favored by sexual selection. We used a mathematical approach in which males alone provide parental care and exhibit a non-care trait that is preferred in mate choice. Using this approach, we demonstrate that life-history characteristics (stage-specific mortality, fertilization success, gamete numbers) can interact with sexual selection to influence the evolution of paternal care and/or a preferred non-care trait. In particular, whether (1) adult mortality, egg mortality, and fertilization success are high versus low and (2) a tradeoff exists between paternal care and a non-care preferred trait will influence whether selection most strongly favors additional paternal care or a non-care preferred trait. In general, we would expect strong selection for more male care when it is preferred in mate choice. In some cases, mate preferences for paternal care can inhibit selection for a preferred non-care trait. Mate preferences for paternal care can also broaden the life-history conditions under which we would expect the elaboration of male care to occur.

Unifying cornerstones of sexual selection: operational sex ratio, Bateman gradient and the scope for competitive investment.

What explains variation in the strength of sexual selection across species, populations or differences between the sexes? Here, we show that unifying two well-known lines of thinking provides the necessary conceptual framework to account for variation in sexual selection. The Bateman gradient and the operational sex ratio (OSR) are incomplete in complementary ways: the former describes the fitness gain per mating and the latter the potential difficulty of achieving it. We combine this insight with an analysis of the scope for sexually selected traits to spread despite naturally selected costs. We explain why the OSR sometimes does not affect the strength of sexual selection. An explanation of sexual selection becomes more logical when a long 'dry time' ('time out', recovery after mating due to e.g. parental care) is understood to reduce the expected time to the next mating when in the mating pool (i.e. available to mate again). This implies weaker selection to shorten the wait. An integrative view of sexual selection combines an understanding of the origin of OSR biases with how they are reflected in the Bateman gradient, and how this can produce selection for mate acquisition traits despite naturally selected costs.

Cascading effects of pre-adult survival on sexual selection.

Sexual selection influences broad-scale patterns of biodiversity. While a large body of research has investigated the effect of mate competition on sexual selection, less work has examined how pre-adult life history influences sexual selection. We used a mathematical framework to explore the influence of pre-adult survival on sexual selection. Our model suggests that pre-adult male mortality will affect the strength of sexual selection when a fixed number of adult males have an advantageous mate-acquisition trait. When a fixed number of males have an advantageous mate-acquisition trait, sexual selection is expected to increase when pre-adult mortality is relatively low. By contrast, if a fixed proportion (rather than number) of adult males have a mate-acquisition trait, pre-adult male mortality is not expected to affect the strength of sexual selection. Further, if the advantageous mating trait affects pre-adult survival, natural and sexual selection can interact to influence the overall selection on the mating trait. Given that pre-adult mortality is often shaped by natural selection, our results highlight conditions under which natural selection can have cascading effects on sexual selection.

Resource acquisition and pre-copulatory sexual selection.

Sexual selection influences the evolution of phenotypic traits and contributes to patterns of biodiversity. In many animals, mating involves sequential steps. Often, individuals must secure resources that are essential for mating (nests, territories, food), and then after securing a resource, individuals engage in competition for access to limited opposite sex mates and gametes. A large body of empirical research and some verbal models have illustrated that resource acquisition can influence sexual selection. In general, though, we lack a priori predictions of when and how resource acquisition will influence sexual selection. Here, we use a mathematical framework to explore the link between resource acquisition and sexual selection on an advantageous mate-acquisition trait across biologically relevant trade-off scenarios. Our findings provide a set of testable predictions of how resource acquisition can influence sexual selection on mating traits. In general, selection on mate-acquisition traits is expected to be heavily influenced by: (1) the episode of selection considered, and in particular, whether one considers selection associated with the mating pool only or selection associated with both the mating pool and pre-mating pool; (2) whether resource-acquisition and mate-acquisition traits are positively associated or whether they trade off; and (3) the proportion of males with the resource- and mate-acquisition traits.

More than just noise: Chance, mating success, and sexual selection.

Chance plays a critical but underappreciated role in determining mating success. In many cases, we tend to think of chance as background noise that can be ignored in studies of mating dynamics. When the influence of chance is consistent across contexts, chance can be thought of as background noise; in other cases, however, the impact of chance on mating success can influence our understanding of how mates are acquired and how sexual selection operates. In particular, when the importance of chance covaries with biological or ecological factors in a systematic manner-that is, when chance becomes consistently more or less important under certain conditions-then chance is important to consider if we want to fully understand the operation of mate acquisition and sexual selection. Here, we present a model that explores how chance covaries with factors such as sex ratio, adult population size, and mating regime in determining variation in mating success. We find that in some cases, chance covaries with adult population size and the operational sex ratio to create variation in mating success. We discuss how chance can influence our more general understanding of the operation of mating dynamics and sexual selection.

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.

Visualizing connectivity of ecological and evolutionary concepts-An exploration of research on plant species rarity.

Understanding the ecological and evolutionary factors that influence species rarity has important theoretical and applied implications, yet the reasons why some species are rare while others are common remain unresolved. As a novel exploration of scientific knowledge, we used network analysis conceptually to visualize the foci of a comprehensive base of >800 studies on plant species rarity within the context of ecology and evolution. In doing so, we highlight existing research strengths that could substantiate novel syntheses and gaps that could inspire new research. Our results reveal strong integrated foci on population dynamics with other ecological concepts. In contrast, despite the potential for ecological and evolutionary processes to interact, few studies explored the interplay of environmental factors and microevolutionary patterns. The cellular and molecular biology, physiology, and plasticity of rare plant species within both ecological and evolutionary contexts similarly provide avenues for impactful future investigations.

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.

Parents benefit from eating offspring: density-dependent egg survivorship compensates for filial cannibalism.

Why should animals knowingly consume their own young? It is difficult to imagine many circumstances in which eating one's own young (i.e., filial cannibalism) actually increases an individual's fitness; however, filial cannibalism commonly co-occurs with parental care in fishes. The evolutionary significance of filial cannibalism remains unclear. The most commonly accepted explanation is that filial cannibalism is a mechanism by which caring males gain energy or nutrients that they reinvest into future reproduction, thereby increasing net reproductive success. There is mixed support for this hypothesis and, at best, it can only explain filial cannibalism in some species. A recent alternative hypothesis suggests that filial cannibalism improves the survivorship of remaining eggs by increasing oxygen availability, and thus increases current reproductive success. This theory has received little attention as of yet. We evaluated the hypothesis of oxygen-mediated filial cannibalism in the sand goby by examining the effect of oxygen and egg density on the occurrence of filial cannibalism, evaluating the effects of partial clutch cannibalism on the survivorship of remaining eggs, and comparing potential costs and benefits of filial cannibalism related to the net number of eggs surviving. Indeed, we found that oxygen level and egg density affected the occurrence of cannibalism and that simulated partial clutch cannibalism improved survivorship of the remaining eggs. Additionally, because increased egg survivorship, stemming from partial egg removal, compensated for the cost of cannibalism (i.e., number of eggs removed) at a range of cannibalism levels, filial cannibalism potentially results in no net losses in reproductive success. However, oxygen did not affect egg survivorship. Thus, we suggest a more general hypothesis of filial cannibalism mediated by density-dependent egg survivorship.

Population-Level Density Dependence Influences the Origin and Maintenance of Parental Care.

Parental care is a defining feature of animal breeding systems. We now know that both basic life-history characteristics and ecological factors influence the evolution of care. However, relatively little is known about how these factors interact to influence the origin and maintenance of care. Here, we expand upon previous work and explore the relationship between basic life-history characteristics (stage-specific rates of mortality and maturation) and the fitness benefits associated with the origin and the maintenance of parental care for two broad ecological scenarios: the scenario in which egg survival is density dependent and the case in which adult survival is density dependent. Our findings suggest that high offspring need is likely critical in driving the origin, but not the maintenance, of parental care regardless of whether density dependence acts on egg or adult survival. In general, parental care is more likely to result in greater fitness benefits when baseline adult mortality is low if 1) egg survival is density dependent or 2) adult mortality is density dependent and mutant density is relatively high. When density dependence acts on egg mortality, low rates of egg maturation and high egg densities are less likely to lead to strong fitness benefits of care. However, when density dependence acts on adult mortality, high levels of egg maturation and increasing adult densities are less likely to maintain care. Juvenile survival has relatively little, if any, effect on the origin and maintenance of egg-only care. More generally, our results suggest that the evolution of parental care will be influenced by an organism's entire life history characteristics, the stage at which density dependence acts, and whether care is originating or being maintained.

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.

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.

The evolution of social interactions changes predictions about interacting phenotypes.

In many traits involved in social interactions, such as courtship and aggression, the phenotype is an outcome of interactions between individuals. Such traits whose expression in an individual is partly determined by the phenotype of its social partner are called "interacting phenotypes." Quantitative genetic models suggested that interacting phenotypes can evolve much faster than nonsocial traits. Current models, however, consider the interaction between phenotypes of social partners as a fixed phenotypic response rule, represented by an interaction coefficient (ψ). Here, we extend existing theoretical models and incorporate the interaction coefficient as a trait that can evolve. We find that the evolution of the interaction coefficient can change qualitatively the predictions about the rate and direction of evolution of interacting phenotypes. We argue that it is crucial to determine whether and how the phenotypic response of an individual to its social partner can evolve to make accurate predictions about the evolution of traits involved in social interactions.

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.

Hurry-up and hatch: selective filial cannibalism of slower developing eggs.

Filial cannibalism (the consumption of one's own offspring) is thought to represent an adaptive strategy in many animals. However, little is known about the details of which offspring are consumed when a parent cannibalizes. Here, we examined patterns of within-brood filial cannibalism in the sand goby (Pomatoschistus minutus). Males spawned sequentially with two females, and we asked whether males cannibalized selectively with regard to egg size or the order in which eggs were received. Males preferentially consumed the larger eggs of the second female they spawned with. Because larger eggs took longer to hatch, and because female 2's eggs were up to 1 day behind those of female 1, such preferential cannibalism might allow males to decrease the time spent caring for the current brood and re-enter the mating pool sooner. More work is needed to understand the fitness consequences of such selective cannibalism.