LIFE HISTORY AND THE EVOLUTION OF PARENTAL CARE

Authors


Abstract

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.

Parental care is a defining feature of animal breeding systems and has received immense empirical and theoretical attention during the last several decades. Much work has focused on explaining which sex should provide care (Williams 1966; Baylis 1981; Gross and Sargent 1985; Queller 1997; McNamara et al. 2000; Kokko and Jennions 2008), how much care should be provided (Carlisle 1982; Winkler 1987; Clark and Ydenberg 1990; Westneat and Sherman 1993; Gross 2005), and describing patterns of parental behavior in species exhibiting care (general reviews in Ridley 1978; Tallamy 1984; Clutton-Brock 1991; Rosenblatt and Snowdon 1996; Reynolds et al. 2002; Rosenblatt 2003; Gross 2005). No doubt, the diversity of parental care strategies in species that provide care is astounding, ranging from minimal care (e.g., incidental guarding of eggs spawned in mating territories, Echelle 1973) to extreme care that ultimately results in the death of the parent (e.g., sacrificial maternal care in spiders, Evans 1998). Equally striking, however, is the diversity in whether parental care is provided at all. Indeed, there is remarkable variation in the presence/absence of parental care within and between higher taxonomic groups (reviewed in Clutton-Brock 1991), and parental care is thought to have evolved independently multiple times (discussed in Rosenblatt and Snowdon 1996). For example, in ray-finned fish alone, phylogenetic analyses suggest that the independent emergence of parental care has occurred at least 33 times (Mank et al. 2005). Despite such diversity in the emergence of care, the origin of parental care has received relatively little theoretical and empirical attention.

Most generally, parental care is expected to evolve from an ancestral state of no care when the fitness benefits to a caring parent (e.g., increased offspring survival and/or quality) outweigh the costs of providing care (e.g., decreased survival and future reproductive success). Thus, care is likely to be favored when (1) the relative benefits of care are high (e.g., Wilson (1975) suggested this will occur in environments with limited food availability and/or high predation) and (2) the costs of providing care are relatively low (e.g., if parental care is preferred in mate choice, e.g., Baylis 1981; Tallamy 2000). As parental care requires an association between parents and offspring, care is expected to be favored when parents recognize (Pfennig 1997; Clutton-Brock 1991; West et al. 2007) or regularly encounter their offspring (Lion and van Baalen 2007). For example, altruistic behaviors such as parental care are more likely to be favored in populations that are ‘viscous’ (i.e., have low dispersal; Hamilton 1964; van Baalen and Jansen 2006; West et al. 2007) if the benefits of care are not outweighed by costs associated with increased competition among closely related individuals (Kelly 1992; West et al. 2002). Some studies have also focused on the relationship between the evolution of parental care and ectothermy (Hopson 1973; Case 1978; Gross and Shine 1981; discussed in Clutton-Brock 1991), fertilization mode (Werren et al. 1980; Gross and Shine 1981; Beck 1998; Mank et al. 2005), and egg size (Smith and Fretwell 1974; Shine 1978; Sargent et al. 1987; Winemiller and Rose 1992). However, as of yet, no studies have identified the most general life-history conditions (i.e., stage-specific mortality, maturation, and reproductive rates) that are likely to favor the evolution of parental care (or other altruistic behaviors among closely related kin). Using a verbal argument based on r- and k-selection theory (following Pianka 1970), Stearns (1976) predicted that low juvenile relative to adult survival will be correlated with increased need for parental care, and in general, organisms with relatively long life spans will be more likely to exhibit parental care. Beyond this though, there has been no explicit examination of the relationship between the origin of parental care and stage-specific life-history characteristics.

Here, we use a mathematical model to explore the general life-history conditions favoring the evolution of parental care. We quantify the relationship between the origin of parental care from an ancestral state of no care in relation to (1) egg, juvenile, and adult mortality rates, (2) adult reproductive rate, (3) egg maturation rate, and (4) the duration of the juvenile stage. In doing so, we identify the basic life-history conditions under which care is most likely to evolve, and we discuss our findings in relation to natural patterns of care.

Methods

Using an evolutionary ecology approach (Metz et al. 1992, 1996; Dieckmann and Law 1996; Vincent and Brown 2005; Otto and Day 2007), we allow a rare mutant that exhibits parental care to invade a resident population in which parental care does not occur. The resident strategy is assumed to be in equilibrium and the alternative parental care strategy invades from rare into the population. Building upon previous work (described in Klug and Bonsall 2007), we assume a stage-structured system in which individuals pass through egg and juvenile stages and then mature and reproduce as adults (as such a stage-structured system is likely to be applicable to a range of animals). We assume that the mutant and the resident experience the same baseline conditions (i.e., both resident and mutant have the same death, maturation, and reproductive rates when no care is provided). Parental care is then assumed to be associated with benefits to offspring (i.e., increased survival beyond the baseline survival rate in the absence of care) and costs to the parent providing it (i.e., decreased parental survival and future reproduction relative to the no care scenario; costs and benefits of care described in detail below). For a series of fixed benefits and costs of parental care that are likely to result in net fitness benefits (described below), we explore the conditions under which parental care is most likely to be able to invade a resident strategy of no care.

As mentioned previously, parental care requires association between parents and offspring. It is important to note that we assume such an association, but do not specify how this association between parent and offspring arises. Although not explicit in our model, such an association could arise if parents recognize their offspring (for examples of kin recognition see Pfennig 1997; Evans 1998; Fellowes 1998; Evans 1999; Komdeur et al. 2008) or if parents and offspring tend to be spatially clumped (e.g., because of delayed offspring dispersal). For example, in many species, eggs are spawned in breeding territories, creating a close physical association between parents and offspring; such breeding territories are hypothesized to have preceded the evolution of care in fish and birds (Williams 1975; Wesolowski 1994; see also Lion and van Baalen for discussion of spatial structure and the evolution of care). The model dynamics described below are consistent with either of these scenarios.

MODEL DYNAMICS

Individuals pass through an egg (E), juvenile, and adult stage (A). Eggs increase as adults reproduce and decrease as eggs mature and as eggs die, such that

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where r represents the rate of egg fertilization (i.e., mean reproductive rate of adults), dE represents death rate of eggs, and mE is the rate at which eggs mature. We assume logistic population growth, where K represents population carrying capacity, and density-dependence associated with resource competition affects adult reproduction (i.e., the rate of fertilization). Adults in the population increase as eggs mature and survive the juvenile stage, and decrease as adults die, such that

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where τ is a time delay representing the length of the juvenile stage, σJ is survival rate through the juvenile stage, and dA is the density-independent death rate of adults.

The equilibrial densities are thus

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and

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COSTS AND BENEFITS OF PARENTAL CARE AND INITIAL ALLOCATION INTO EGGS

Parents can affect offspring survival and quality by (1) investing energy and nutrients into eggs (which we refer to as initial egg allocation), which can then affect subsequent survival and (2) providing postoviposition parental care behavior (which we refer to simply as parental care) to offspring in one or more life-history stages. Both initial egg allocation and parental care can have a range of benefits to offspring and costs to parents. Here, we consider three general parental care strategies: no parental care (Case 1; i.e., the resident strategy), parental care of eggs (Case 2), and parental care of eggs and juveniles (Case 3). The different care strategies are represented through the incorporation of appropriate trade-offs into the resident and mutant dynamics (described below and in Table 1). The level of parental care is approximated by a fixed value (Table 1), and can be thought of as some average level of care that a mutant adult provides to its mutant offspring. Egg death rate is used as our proxy of initial egg allocation. Specifically, parental care is assumed to increase offspring survival during the stage in which it is provided; in other words, as the level of care to eggs (Case 2) or eggs and juvenile (Case 3) increases, the survival of eggs and/or juveniles will increase (Table 1). Providing care behavior is assumed to be costly to parents, and as the level of care increases, adult survival declines (i.e., death rate increases) and reproductive rate decreases (Table 1). Likewise, initial egg allocation is also expected to be costly to parents, such that as initial egg allocation increases, adult survival and reproductive rates decrease. Initial egg allocation affects egg survival, and in some cases, benefits of initial egg allocation might extend beyond the egg stage. Thus, we consider the case in which initial egg allocation by parents affects only egg survival (Case 1a, 2a, and 3a; Table 1) versus the scenario in which initial egg allocation affects offspring quality, such that high investment in eggs improves both egg and subsequent juvenile survival (Case 1b, 2b, and 3b; Table 1). In all cases, we assume nonlinear trade-offs (described in Table 1), as nonlinear trade-offs are often thought to be biologically realistic and have been used in previous models of parental investment and care (e.g., Smith and Fretwell 1974; Sargent et al. 1987; Winkler 1987), but the general patterns were qualitatively similar if linear trade-offs were used (see also Klug and Bonsall 2007). Although the trade-off functions described in Table 1 provide some insight into whether it is possible for various levels of parental care to result in net fitness benefits, these trade-off functions alone do not provide information on whether parental care will actually be able to invade a resident strategy of no care and persist given the stage-structured life-history conditions and the ecological dynamics of the system. Information on invasion of different strategies necessitates further analyses and is described below.

Table 1.  Life-history trade-offs associated with parental care (c) and initial investment in eggs (1−dE0). We consider both high (a=6, solid line) and low (a=2, dashed line) levels of parental care benefits.
ParameterCaseExample of trade-offs associated with care
1. No care2. Parental care of eggs3. Parental care of eggs and juveniles
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INVASION DYNAMICS AND FITNESS

The dynamics of the rare mutant are given by the following equations and by incorporating the relevant trade-offs into the mutant and resident dynamics (Table 1):

image(5)
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where A* is the equilibrial abundance of the resident adult population. The other parameters are as described previously, and subscript m denotes the new mutant strategy that exhibits parental care. As mentioned previously, to consider the invasion of parental care from an ancestral state of no care, we consider the case in which a rare adult mutant is present and able to provide parental care to its offspring. Thus, we assume that mutant parents are associated with their offspring (e.g., due spatial clumping or kin recognition, as discussed above) and remain alive long enough to provide care to young.

Parental care, which is only provided by the mutant parent to the mutant offspring, is assumed to occur locally (Table 1). In contrast, competition for resources that limit reproduction (e.g., food, mating opportunities) are assumed to occur more globally; the mutant is assumed to be rare in the population, and thus, density-dependence operating on adult mutant reproduction occurs through competition with the resident (eqn. 5). The lifetime fitness of the mutant can then be found by taking the determinant of:

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and solving the resulting characteristic equation (Appendix) for λ (i.e., the fitness of the mutant strategy relative to that of the resident; see also Metz et al. 1992 and Vincent and Brown 2005). As mentioned, we are interested in the general conditions that favor the evolution of parental care when a rare mutant that provides parental care is present in a population. Thus, we assume that all baseline conditions (i.e., all parameter values) are identical for the mutant and resident strategy (see also Klug and Bonsall 2007). We then calculate the fitness of the mutant strategy relative to that of the resident strategy for a series of fixed benefits and costs of parental care (Table 1) and in relation to varying life-history parameters (i.e., egg death rate, adult death rate, juvenile survival, egg maturation rate, reproductive rate, duration of the juvenile stage) and the level of care provided. In doing so, we (1) identify the life-history conditions under which parental care is most likely to result in net fitness benefits given the stage-structured life history of the organism and the underlying ecological dynamics of the system, and (2) for the cases in which care can invade, we determine the relative amount of care that is likely to be provided for a range of life-history conditions during the early evolution of care. All patterns were then confirmed by pairwise invasion analyses in which we (1) used the fitness function of the mutant to calculate the evolutionary stable state(s) (i.e., when the rate of change in fitness is zero) and (2) performed mutual invasion analyses by evaluating when the fitness function is greater than zero (using a Newton–Raphson algorithm with the resident dynamics (A*) set at equilibrium) for different values of various life-history traits (i.e., egg death rate, juvenile survival, adult death rate, reproductive rate, egg maturation rate; see also Klug and Bonsall 2007 for additional details of invasion analyses). In all cases, the invasion dynamics were consistent with the results obtained from calculating the relative fitness of the parental care strategy, and as such we present only the results associated with relative fitness.

Results

FITNESS OF PARENTAL CARE UNDER WEAK SELECTION

The formula for the fitness of the mutant strategy is given in the Appendix; fitness for each strategy can be determined by incorporating the corresponding life-history trade-offs (Table 1). A limiting case for the model can be derived when selection is assumed to be weak (i.e., when the difference between the resident and mutant fitness is small and λ→ 0). This provides insight into which life-history traits are most likely to influence the invasion of care. When selection is weak, fitness of the mutant strategy is positive when:

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This suggests that even under weak selection, nearly all life-history traits considered (adult death rate, egg death rate, egg maturation rate, adult reproductive rate, juvenile survival) will be important determinants of fitness. In contrast, the duration of the juvenile stage (which does not affect fitness under weak selection, eqn. 8) is only expected to affect mutant fitness (and hence invasion) when selection is relatively strong. Under weak selection, density-dependent competition and the size of the resident population are also expected to be important determinants of mutant fitness and invasion, unless the mutant's carrying capacity equals the equilibrium density of adults exhibiting the resident strategy (see also Klug and Bonsall 2007 for discussion of how varying carrying capacities between the mutant and resident strategy can affect the invasion of care). Additionally, when selection is weak and the mutant's carrying capacity equals the equilibrium density of adults exhibiting the resident strategy, egg death rate, adult death rate, and egg maturation rate are expected to be the most important determinants of mutant fitness and invasion (eqn. 8). Below, we explore the effect of each life-history trait on the invasion of parental care for the cases in which selection is both strong and weak (i.e., when the benefits of care are relatively large vs. small) for the life-history scenarios of interest (Cases 1–3 in the Methods section).

EGG DEATH RATE

Parental care of eggs (Case 2 in the Methods section) is most strongly favored when egg survival is low in the absence of care (Fig. 1). When the benefits of care to eggs are weak (described in Table 1), the overall fitness benefits associated with care are greatest at high to intermediate levels of egg death rate, and care is unlikely to evolve when baseline egg death rate is low (Fig. 1A, dashed line). When the benefits of care to eggs are high, care results in fitness benefits over a broader range of baseline egg death rates, but is most strongly selected for when all eggs die in the absence of care (Fig. 1A, solid line). As egg death rate increases, the level of parental care provided is expected to increase (Fig. 1B). In particular, when the benefits of care are relatively weak and baseline egg death rate is high, a relatively high level of care must be provided for care to result in fitness benefits (Fig. 1B). These patterns (Fig. 1A) are qualitatively identical when there is a positive relationship between initial investment in eggs and subsequent juvenile survival (Case 2b in the Methods section). However, when there is a positive relationship between initial investment in eggs and subsequent juvenile survival, all levels of care result in fitness benefits with respect to egg death rate, although selection will favor stronger levels of care as baseline egg death rate increases (as in Fig. 1B).

Figure 1.

Fitness benefits of parental care in relation to baseline egg death rate. (A) Parental care of eggs is favored at relatively high egg death rates when the benefits of care are high (solid line; see also Table 1) and low (dashed line; see also Table 1). (B) The level of parental care provided to eggs is expected to increase as egg death rate increases (low benefits of care shown here, although the results are qualitatively the same for high benefits of care). (C) Parental care of eggs and juveniles is favored at a range of egg death rates and is most beneficial when egg death rate is high in the absence of care for both high (solid line) and low benefits (dashed line) of care. (D) The level of parental care provided to eggs and juveniles is expected to increase as egg death rate increases (low benefits of care shown here, although the results are qualitatively similar for high benefits of care) (unless otherwise noted, c= 0.4, mE= 0.1, r0= 6, dA0= 0.5, K= 50, σJ0= 0.01, τ= 0.1).

Similarly, when parents provide care during both egg and juvenile stages (Case 3 in the Methods section), fitness benefits of care are maximized at very high baseline egg death rates (Fig. 1C). However, in comparison to scenario above (i.e., egg-only care), egg death rate is relatively less important in the evolution of care when care extends into the juvenile stage. Indeed, parental care of both eggs and juveniles has the potential to evolve over a broad range of egg death rates even when the benefits of care are relatively weak (Fig. 1C, dashed line). Likewise, although there will be selection for stronger care at higher egg death rates, all levels of parental care potentially result in fitness benefits when care extends beyond the egg stage (Fig. 1D). These patterns were qualitatively identical when initial investment in eggs affects subsequent juvenile survival (Case 3b in the Methods section).

JUVENILE SURVIVAL

The fitness benefits associated with parental care are unaffected by juvenile survival when parental care is only provided during the egg stage (Fig. 2A). When parental care is provided during the egg and juvenile stages, care results in the greatest fitness benefits when juvenile survival is low in the absence of care (Fig. 2B). However, parental care results in fitness benefits across most values of juvenile survival, especially when the benefits of care are relatively high (Fig. 2B). In general, there is no relationship between juvenile survival and the level of care that is provided (Fig. 2C). For a given juvenile survival rate, all levels of care will result in approximately equal fitness benefits (Fig. 2C). These patterns are qualitatively identical when there was a positive relationship between initial investment in eggs and subsequent juvenile survival.

Figure 2.

Fitness benefits of parental care in relation to baseline juvenile survival. (A) Parental care of eggs is unaffected by baseline juvenile survival for both high benefits of care (solid line) and low benefits of care (dashed line); (B) Care provided during the egg and juvenile stage results in the greatest fitness benefits when baseline juvenile survival is low (high benefits of care, solid line; low benefits of care, dashed line). (C) The level of parental care provided to eggs and juveniles is unaffected by baseline juvenile survival (low benefits of care shown here, although the results are qualitatively similar for high benefits of care) (unless otherwise noted, c= 0.4, mE= 0.1, r0= 6, dA0= 0.5, K= 50, dE0= 0.5, τ= 0.1).

ADULT DEATH RATE

Parental care of eggs is favored by relatively high adult death rates (Fig. 3A), and in particular, care is unlikely to evolve when adult death rate is low and the benefits of care are relatively small (Fig. 3A, dashed line). As adult death rate increases, the level of care exhibited is expected to increase (Fig. 3B). When parental care is provided to both eggs and juveniles, care results in fitness benefits at all levels of adult death rate, but it is most strongly favored when adult death rate is high (Fig. 3C). As with the scenario of parental care of only eggs, care of both eggs and juveniles is expected to increase as adult death rate increases (Fig. 3D). However, when care is provided to both eggs and juveniles, all levels of care will result in positive fitness with respect to adult death rate. These patterns were unchanged when we assumed a relationship between initial investment in eggs and subsequent juvenile survival.

Figure 3.

Fitness benefits of parental care in relation to baseline adult death rate. (A) Parental care of eggs is favored at high adult death rates (high benefits of care, solid line; low benefits of care, dashed line) and is unlikely to evolve when adult death rate is low and the benefits of care are low. (B) The level of care provided to eggs is expected to increase as adult death rate increases (low benefits of care shown here, although the results are qualitatively similar for high benefits of care). (C) Care of eggs and juveniles can result in fitness benefits at all levels of adult death rates, but is most strongly favored at high levels of adult death rates. (D) The level of care provided to eggs and juveniles is expected to increase as adult death rate increases (low benefits of care shown here, although the results are qualitatively similar for high benefits of care) (unless otherwise noted, c= 0.4, mE= 0.1, r0= 6, σJ0= 0.01, K= 50, dE0= 0.5, τ= 0.1).

EGG MATURATION RATE

Parental care of eggs is only favored when eggs develop relatively slowly (i.e., at low values of egg maturation rate) and egg-only care is unexpected to evolve when eggs mature quickly (Fig. 4A). As egg maturation rate increases, the level of care provided is expected to decrease (Fig. 4B). Similarly, when there is a positive relationship between initial investment in eggs and subsequent juvenile survival, parental care of only eggs or of both eggs and juveniles will be favored only at low levels of egg maturation rate, and the level of care provided is expected decrease as egg maturation rate increases. However, the patterns were strikingly different for the scenario in which parental care is provided to both eggs and juveniles and there is no relationship between initial investment in eggs and juvenile survival (Case 3a in the Methods section). In this case, care of eggs and juveniles is favored at all levels of egg maturation rate, and results in the greatest fitness benefits when egg maturation rate is high (Fig. 4C). Additionally, under these conditions (i.e., Case 3a in the Methods section), the level of care provided to eggs and juveniles is expected to increase as egg maturation rate increases (Fig. 4C).

Figure 4.

Fitness benefits of parental care in relation to egg maturation rate. (A) Parental care of eggs only results in fitness benefits when egg maturation rate is low (high benefits of care, solid line; low benefits of care, dashed line). (B) The level of care provided to eggs is expected to decrease as egg maturation rate increases (low benefits of care shown here). (C) Care of eggs and juveniles results in the greatest fitness benefits when egg maturation rate is high (high benefits of care, solid line; low benefits of care, dashed line). (D) The level of care provided to eggs and juveniles is expected to increase as egg maturation rate increases (low levels of care shown here) (unless otherwise noted, c= 0.4, r0= 6, σJ0= 0.01, K= 50, dE0= 0.5, dA0= 0.5, τ= 0.1).

DURATION OF JUVENILE STAGE

The duration of the juvenile stage has very little effect on the fitness benefits associated with parental care of eggs (Fig. 5A), regardless of whether there is a positive relationship between initial investment in eggs and subsequent juvenile survival. This pattern is qualitatively identical for the case of parental care that extends through the juvenile stage when initial investment in eggs affects juvenile survival. However, when initial investment in eggs does not affect juvenile survival, there is a somewhat greater effect of the duration of the juvenile stage on fitness benefits associated with care of eggs and juveniles. As with the previous scenarios, care of eggs and juveniles is expected to result in net benefits across all values of juvenile stage duration; however, in this case, care is more strongly favored when the duration of the juvenile stage is relatively short (Fig. 5B). Additionally, the level of care provided is expected to decrease as the duration of the juvenile stage increases (Fig. 5C).

Figure 5.

Fitness benefits of parental care in relation to the duration of the juvenile stage. (A) Parental care of eggs has the potential to be beneficial at a range of juvenile stage durations for both high and low benefits of care (solid and dashed lines, respectively). (B) When there is no relationship between initial egg investment and juvenile survival, parental care of eggs and juveniles is most strongly favored when the duration of the juvenile stage is relatively short (high benefits of care, solid line; low benefits of care, dashed line), and (C) the level of care provided to eggs and juveniles is expected to decrease as the duration of the juvenile stage increases (low benefits of care shown here) (unless otherwise noted, c= 0.4, mE= 0.1, r0= 6, σJ0= 0.01, K= 50, dE0= 0.5, dA0= 0.5).

ADULT REPRODUCTIVE RATE

Finally, there was no effect of adult reproductive rate on the fitness benefits associated with care under any of the scenarios considered (Fig. 6). Indeed, care is likely to be favored under all values of adult reproductive rate, and therefore, the evolution of care is influenced by factors other than adult reproductive rate (e.g., egg and adult death rates, juvenile survival, as discussed above) under the conditions of this model.

Figure 6.

Fitness benefits of parental care in relation to adult reproductive rate. Parental care of eggs is potentially beneficial across a range of adult reproductive rates (high benefits of care, solid line; low benefits of care, dashed line) (unless otherwise noted, c= 0.4, mE= 0.1, σJ0= 0.01, K= 50, dE0= 0.5, dA0= 0.5, τ= 0.1).

Discussion

Here, we demonstrate that general life-history conditions are likely to affect the origin of parental care. Care will only evolve when the fitness benefits outweigh the costs, and parental care is most likely to be favored when (1) egg death rate in the absence of care is high, (2) juvenile survival in the absence of care is low (for the scenario in which care extends into the juvenile stage), (3) adult death rate is relatively high, (4) egg maturation rate is low (see Fig. 4B and C regarding exception), and (5) the duration of the juvenile stage is relatively short (Table 2). However, the relative importance of each of the conditions described above depends upon the specific type of care provided (i.e., egg only vs. egg and juvenile care), the relationship between initial allocation in eggs and subsequent offspring survival, and the magnitude of the benefits of parental care. For example, when the benefits of care are relatively low, parental care of eggs is only likely to be favored when egg maturation rate is low and baseline egg and adult death rates are relatively high (Table 3). In contrast, care is more likely to be favored when it is provided for both eggs and juveniles, and adult death rate becomes relatively unimportant when the benefits of egg-only care are high and/or when care extends beyond the egg stage (Table 3). Likewise, when care is provided to both eggs and juveniles and there is no effect of initial egg allocation on subsequent juvenile survival (i.e., care is the only way in which parents can modify juvenile survival), the only life-history condition necessary for the evolution of care is the presence of some juvenile mortality in the absence of care (Table 3).

Table 2.  Summary of the conditions that are predicted to favor the evolution of parental care (from eqns. 5–7) together with some related previous findings.
Life-history conditions favoring parental careExceptionsRelated previous findings
1. High egg death rate Parental care in invertebrates is associated with environments in which offspring are likely to die in absence of care (reviewed in Clutton-Brock 1991, Ch. 7).
2. Low juvenile survivalOnly when care extends through the juveniles stage; no effect of juvenile survival on egg-only care.Stearns (1976) predicted that low juvenile relative to adult survival will lead to parental care.
3. High adult death rates Short life-span is associated with parental care in fishes (Winemiller and Rose 1992). Stearns (1976) predicted that organisms with a short life span will exhibit less parental care than individuals with a longer life span.
4. Low egg maturation ratesHigh egg maturation rates favor care when care extends through the juvenile stage AND when initial egg investment does not affect subsequent juvenile survival.Slow offspring growth is associated with parental care in fishes (Winemiller and Rose 1992).
Shine (1978) and Sargent et al. (1987) suggested that parents should increase the proportion of time offspring spend in relatively safe developmental stages, which might be those in which care is provided.
5. Short duration of juvenile stage
Table 3.  Life-history conditions (i.e., baseline egg maturation rates mE0, egg death rates dE0, adult death rates dA0, and juvenile survival σJ0) that are predicted from eqns. 5–7 to be most important for determining whether parental care can evolve for various types of parental care (described further in Table 1 and the Methods section).
Scenario
Case 2a,b: Egg-only care, Low benefits of careCase 2a,b: Egg-only care, High benefits of care
&
Case 3a: Egg & juvenile care, High or low benefits of care, no effect of initial egg investment on subsequent juvenile survival
 Case 3b: Egg & juvenile care, High or Low benefits of care, Initial egg investment affects subsequent juvenile survival 
 
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The general predictions stemming from our model are consistent with a range of previous findings (Table 2). For example, Winemiller and Rose (1992) explored the relationships among various life-history traits for 216 North American fish species. They found that highly developed parental care in fish is correlated with a short life span, small adult size, and slow adult and offspring growth, whereas the lack of parental care is correlated with long life span, large adult size, and faster adult and offspring growth (Winemiller and Rose 1992). These findings are consistent with our predicted pattern of care being most strongly favored at high baseline adult death rates and low egg maturation rates. Likewise, the finding that slow egg maturation rates favor the evolution of care is consistent with work by Shine (1978) and Sargent et al. (1987), who suggest that selection should lead parents to increase the proportion of time spent in the safest developmental stage (i.e., the safe harbor hypothesis), and parental care might be one way in which parents increase the safety of and the proportion of time offspring spend in the egg stage. The finding that parental care is more likely to be favored when the duration of the juvenile stage is relatively short is, to our knowledge, not predicted by previous work. However, this pattern makes intuitive sense in terms of the model, because the longer individuals remain in the juvenile stage, the greater their chances of dying are (see also eqn. 7).

With regard to offspring survival, our results suggest that parental care is most likely to evolve when offspring need care the most, i.e., when egg and/or juvenile survival is low in the absence of care. Parental care in invertebrates tends to occur only when care is essential for offspring survival (reviewed in Clutton-Brock 1991), and Stearns (1976) and Clutton-Brock (1991) have previously predicted that parental care is likely to occur when offspring survival is low in the absence of care. Additionally, our model also suggests that organisms with high offspring mortality in the absence of care should provide the greatest amounts of parental care early in the evolution of care. This finding is consistent with work by Dale et al. (1996) and Webb et al. (2002) that suggests that parents should provide the most care to offspring that have low survival in the absence of care. In contrast though, others have suggested that parents should provide more care to relatively high quality offspring that are, for example, likely to have high survival (Carlisle 1982, 1985).

In contrast to ideas stemming from previous theory (e.g., Pianka 1970), we found that baseline adult reproductive rate is unlikely to have strong effects on the origin of parental care. Indeed, our results suggest that parental care is likely to evolve at a range of reproductive rates, and this prediction is consistent with the prevalence of parental care in animals with diverse rates of reproduction (e.g., discussed in relation to patterns of care in Ch. 7 of Clutton-Brock 1991). It is important to note that this finding does not suggest that costs of care associated with future parental reproduction are unimportant. Rather, the potential importance of costs associated with future reproduction for the evolution of care are independent of the baseline adult reproductive rate experienced. Thus, our results suggest that parental care has the potential to evolve in organisms experiencing both fast and slow rates of reproduction.

In summary, we have highlighted a range of general life-history conditions that are most likely to favor the initial evolution of parental care (Tables 2 and 3). Offspring characteristics (e.g., maturation and survival rates) have the strongest influence on the potential for care to evolve, although adult mortality can also limit the evolution of care under some conditions. The results of our model provide a baseline set of general, testable predictions regarding when we would expect parental care to evolve initially (e.g., Table 2). In the future it will be important to compare the predictions of our model with patterns of care in relation to basic life-history conditions in nature and also to extend the model to reflect the biological complexity of a range of species. We have not incorporated the complexities associated with more specific forms of care (e.g., female, male, or biparental care), conflict between the sexes, parent-offspring conflict, ecological interactions, or details of kin recognition and/or spatial structure in the current model. This is a limitation of the modeling approach used, and it is likely that these additional dynamics will influence the relationship between life-history traits and the origin of some form of care (Williams 1966; Trivers 1972, 1974; Klug and Bonsall 2007; Lion and van Baalen 2007). Additionally, our model is focused solely on the early evolution of parental care. Exploring the conditions associated with the maintenance of care is a critical avenue for future research. In particular, it will be important to assess the conditions that favor the maintenance of parental care using a framework that accounts for density- and frequency-dependent care behavior, as well as a range of ecological feedbacks that are likely to occur once care becomes more prevalent in a population. A great deal of previous work has focused on which sex should provide care (Williams 1966; Baylis 1981; Gross and Sargent 1985; Queller 1997; McNamara et al. 2000; Kokko and Jennions 2008), evolutionary transitions between different forms of care (Baylis 1981; Gross and Sargent 1985; Burley and Johnson 2002; Reynolds et al. 2002; Tullberg et al. 2002), and the relationship between more specific life-history traits and patterns of care or other altruistic behavior directed at kin (e.g., mode of fertilization: Werren et al. 1980; Gross and Shine 1981; Beck 1998; Mank et al. 2005; egg size: Smith and Fretwell 1974; Shine 1978; Sargent et al. 1987; Winemiller and Rose 1992; ectothermy: Hopson 1973; Case 1978; Gross and Shine 1981; kin recognition: Pfennig 1997; Evans 1998; Fellowes 1998; Evans 1999; West et al. 2007; Komdeur et al. 2008; dispersal and spatial structure: Williams 1975; Kelly 1992; West et al. 2007; Lion and van Baalen 2007). It is likely that this previous work in conjunction with the results presented here will provide insight into understanding patterns of parental care in nature, and facilitate a more general framework of the evolution of parental care.


Associate Editor: R. D. Rausher

ACKNOWLEDGMENTS

The work was supported by National Science Foundation International Research Program Fellowship # 0701286 (to HK) and the Royal Society (to MBB). We are grateful to two anonymous referees for their comments on the manuscript.

Appendix

The fitness of the mutant strategy is obtained by taking the determinant of eqn. 7 and solving the following characteristic equation:

image((A1))

for λ. Fitness of the mutant strategy is thus:

image((A2))

Ancillary