Extreme offspring ornamentation in American coots is favored by selection within families, not benefits to conspecific brood parasites

Correlates of Variation in Chick Coloration.

Our analyses show that there is substantial variation in chick coloration within and across broods. Within broods, there is a clear and strong effect of laying sequence and hatching order on chick color; chick redness increases with hatching order, which reflects laying order. The correlation between hatching (and laying) order and chick color strongly implicates maternal effects as a determinant of within-brood variation in chick color because chicks cannot control the order in which their egg is laid and hatched. There is ample evidence that egg size and egg yolk content vary with laying order in many birds (37, 38). For American coots specifically, Reed and Vleck (39) showed that egg androgen content declines with laying order. Egg size also varies with laying sequence in American coots; the first eggs are typically relatively small, eggs 2 to 5 are the largest, then size declines again for later-laid eggs (40, 41). American coot eggs are known to contain very high amounts of carotenoids in the yolk (42), the highest yet reported for birds, and it is likely that carotenoid content of eggs varies among females and with laying sequence for a female, producing both among- and within-brood variation in chick color. In terms of known effects on chick survival, it is interesting that the relation between egg-laying order and egg androgens is in the opposite direction to the pattern we detected for chick coloration. This might suggest that the underlying mechanisms that connect these different attributes to chick fitness are somewhat independent or have opposing effects.

Chick Ornamentation Is Not Favored through Fitness Females Gain from Brood Parasitism.

A key finding of our study is that potential fitness benefits from brood parasitism is unlikely to explain the extraordinary offspring ornaments in newly hatched American coot chicks, at least in terms of current patterns of variation and selection. Parasitic chicks were less ornamented than nonparasitic chicks, a pattern that held both for comparisons with all nonparasitic offspring in the population and for comparisons restricted with host chicks at parasitized nests. Our previous work showed that parent coots show a strong relative preference for ornamented chicks over experimentally unornamented chicks in their brood (12), so chick ornamentation would only benefit brood parasites if parasitic chicks tended to be more colorful than nonparasitic chicks.

In American coots, parasitic females are not a distinct category of females; instead, most females gain some of their fitness from parasitism and some fitness from typical nesting. It is important to consider that fitness from ornamented chicks could affect more than 1 component of fitness for a given female, and that there may be trade-offs between the fitness from these different components. In our population, most parasitism is by females that also have nests of their own; these females lay their parasitic eggs first and follow with eggs laid in their own nest (33). These nesting parasites could produce more ornamented parasitic chicks in 2 ways. First, parasitic females could be higher-quality females that consistently produce more ornamented offspring generally, both parasitic and in their own nest. Parasites do tend to be older females that lay more total eggs (43), so female quality could provide a feasible mechanism. Second, females could strategically invest in eggs that are destined to be laid parasitically. The observation that parasite chicks are less ornamented than nonparasitic chicks, however, rejects both of these possibilities.

Why don’t female coots make parasitic chicks that are more ornamented, thus increasing the possibility that they would be favored in the host nest? We suggest that laying order effects may preclude strategic investment in eggs destined to be parasitic; within broods, chick ornamentation increases with position in the laying order. Lyon (33) showed that at least 67% of parasitic eggs were laid by females with their own nests (i.e., not floaters), and most (84%) of the parasitic eggs laid by those nesting females were laid before they laid their own clutches in their own nests. Looking in more detail at the specific position in the laying order for the 217 of these parasitic eggs for which we had exact order in the female’s laying sequence, 58% of the parasitic eggs were among the first 3 eggs laid by the female, while 69% were among the first 4 eggs laid by these females.

The chicks from parasitic eggs may be less ornamented simply because they are from the first eggs the female lays in the season. One possibility is that the laying order relation with chick color is a physiological constraint that is difficult to break. Alternatively, it may also be that females cannot predict sufficiently in advance that they will have the opportunity to be parasitic and adjust their egg contents accordingly. Parasitism appears to be opportunistic: Most parasitism involves immediate neighbors and a female can only lay parasitically if she has neighbors with eggs when she is ready to lay because evidence suggests that females do not wait for hosts to become available (43). This opportunism, coupled with the fact that coot eggs take 7 d to form (44), suggests that females might not be able to reliably invest strategically in eggs that end up being laid parasitically because they cannot predict sufficiently in advance whether they will have the opportunity to lay eggs parasitically.

Chick Coloration and Conflicts within Families.

If fitness from parasitism is unlikely to explain coot chick coloration, then any selective benefit to variation in chick ornamentation should be due to selection within families. Such selection could occur for several reasons, some involving conflicts of interest, others cooperation. Our findings suggest that 2 conflicts of interest are unlikely as drivers of chick coloration, but we note that definitive tests are very difficult. The evolution of chick ornamentation could involve parent–offspring conflict (21); chick ornamentation might allow chicks to extract more parental care than is the parents’ interest. Our findings reject this idea because variation within families correlates with position in the egg-laying order, an indication that maternal effects account the within-family variation. However, it is possible that this maternal control represents the outcome of the resolution of past parent–offspring conflict-driven battles (14).

Maternal control of variation within broods is, however, consistent with a second evolutionary conflict, sexual conflict between the parents. Müller et al. (45) suggest that females could use maternal hormones to produce offspring traits that cause the male to increase investment in offspring, and the same logic could apply to other maternal effects generally, including color of eggs or offspring (46, 47). In addition, hatching patterns and hatching order effects like those we observed in coots have also been implicated in sexual conflict: For example, Slagsvold and Lifjeld (23) proposed that different hatching patterns could influence the relative parental investment and costs of the sexes differently, and hence that hatching patterns could drive sexual conflict. In American coots, egg hormones, chick ornamentation, parental feeding rates, and offspring survival all correlate with an egg’s position in the laying order, consistent with the hypothesis that maternal effects or hatching patterns could be driven by sexual conflict. Experimental manipulation of both plumage and hatching patterns are needed to rigorously test the sexual conflict hypothesis. Nonetheless, the present finding—that chick coloration correlates with parental favoritism and investment patterns equally in both sexes—suggests that chick coloration patterns are more likely to reflect tactics that involve parental cooperation than sexual conflict.

Chick Redness Affects Parental Favoritism but Does Not Directly Affect Survival.

A key result of our study was the discovery that variation in chick coloration correlates with parental favoritism in broods with natural hatching patterns. This is an important finding because it suggests that chick coloration—and parental preference for colorful chicks—represents a parental strategy that is adaptive for both parents and is not driven by sexual conflict. Although the female parents control the relation between chick color and egg sequence, a mechanism that could potentially manipulate males into increasing their parental investment, the fact that both parents follow same general pattern of favoritism in terms of relative hatching order (35) and color (present study) suggests that any relation between chick coloration and favoritism benefits both parents.

Some context is necessary to fully appreciate the links between chick coloration, hatching asynchrony, and parental favoritism. Brood reduction is extreme in American coots: On average, parents lose about 50% of their chicks before independence due to starvation, and it is primarily the later-hatching chicks that starve (33, 35). Most chick mortality occurs early after hatching (first 10 d) when parents do not control food allocation but instead feed the first chick that reaches them when the parent finds a prey item. The older chicks get more food, and therefore survive better, because their large size allows them to swim faster and get to parents first. However, starting at about 10 d after the last chick hatches, parents begin to control food allocation and reverse the competitive advantage of the older chicks. Parents use selective aggression toward the older chicks to ensure that the youngest (i.e., latest-hatching) of the remaining chicks get the most food (35). Each parent chooses a single “favorite” chick that receives about 80% of feeds from that parent but receives almost no feedings from the other parent. Most (65%) of these favored chicks were among the last-hatching chicks among the surviving chicks (i.e., chicks surviving to the end of the observation period).

We now add to the previous work on parental favoritism by showing that favorite chicks not only are later-hatched chicks, but they are also more colorful. However, because both chick color and favoritism correlate with hatching position, observations from natural broods alone do not provide convincing evidence that parents are using chick color per se to decide which chicks to feed; some other correlate of hatching order, like chick size, could explain the observed pattern. However, the combined results from our 2 experiments that separately modified chick coloration and hatching asynchrony (ref. 12 and the present study, respectively) together provide convincing evidence that parents are using the color itself, but that hatching position is also important in when parents pay attention to chick color. By experimentally altering chick coloration in the previous study (12), we showed that plumage coloration itself dramatically affects parental feeding decisions, but there was also an interaction with hatching order whereby colorful plumage only benefits later-hatched chicks. In the present study, when we experimentally reduced hatching asynchrony we found that natural levels of variation in chick coloration did not predict which chicks became parental favorites, in striking contrast to the broods with natural levels of asynchrony. Thus, parents use chick color to choose favorites, but only do so when hatching is asynchronous.

Why would parents use chick color to make their decisions about favoritism? One possibility is that color serves as a reliable signal of the chick’s size or age, particularly at the point when parents begin to favor a single chick (12). If this were the case, the relative color of juvenile ornamental may serve as a signal that helps the parent invest parental care in a manner that maximizes both the fitness of the favored offspring and the parent (18, 19). Chick color could provide an honest signal of size or age in 2 ways. First, the strong correlation between color (redness) and egg sequence/hatching day could be used as a cue for relative age of chicks. Second, the color of ornaments may change with increasing chick size due to fading or the decrease in relative density of ornamental plumage with increasing surface area of chicks. In unmanipulated broods, these 2 effects would reinforce each other. In contrast, in our experimental synchrony broods, the color of chicks would be decoupled from the egg sequence and hatching order, but it is yet unknown whether the timing of fading of ornamental traits was correlated with chick size in these broods. Thus, our results suggest that the former mechanism (egg sequence effect) may be sufficient as an honest signal of relative age, although the latter effect (fading/dilution effect) could be an additional, reinforcing mechanism.

The likelihood that chick color eventually changes with age or size, through dilution or fading of the color, raises the issue of the temporal mismatch between when we obtained our color measurement (at hatch) and when parents exert parental control and show completely parental favoritism (around day 10). If chick color changes quickly with age, and if change is sufficiently uncorrelated with hatch color, then our measurement might not be useful for investigating links between chick color and parental favoritism. However, were this to be the case, we should not have found a clear association between color measured at hatch and the likelihood that a chick becomes a parental favorite because random changes in color would obscure rather than produce this clear pattern. This suggests that either hatch color correlates with color when parents exert control and choose their favored chicks (i.e., after day 10), or alternatively, that chick color at hatching begins to bias parental provisioning toward redder chicks in earlier stages but the patterns become more observable during the period of parental favoritism.

Although chick coloration correlates with parental favoritism, we were unable to detect a clear relation between chick coloration and survival in either unmanipulated broods or the mixed synchrony experiments that controlled for the effects of hatching asynchrony. For the unmanipulated broods, the lack of pattern may result because by the time parental favoritism is established, the period of heavy chick mortality has already occurred, and that mortality is almost entirely determined by a chick’s position in the hatching order (34). Moreover, parental favoritism functions to level the playing field for the disadvantaged late-hatched chicks; their increased feeding rate enables them to catch up with their earlier siblings in terms of growth (34). As such, enhanced ornamentation should reduce the mortality rate of these chicks relative to what it would be without the parental favoritism, and experiments may be required to detect survival effects. We have now done 2 such experiments. Our synchrony experiments, which manipulated hatch pattern but not chick coloration, did not yield clear survival patterns. However, when the color variation among chicks was drastically magnified while leaving hatching asynchronous—as in our earlier experimental study where orange plumes were trimmed from half of the chicks in each brood—striking survival patterns did emerge (12). Even in that experiment, however, hatching order still played a role and the plumage experiments only affected the survival of later-hatched chicks in the brood (12). Taken together, all of these observations indicate that the interaction between offspring coloration and parental preference in American coots is strongly dependent on the order in which eggs are produced and hatched within a clutch. Overall, the various patterns we found suggest that extant patterns of variation in chick color make sense in terms of parental care strategies that benefit both the parent and the ornamented offspring.

Conclusions.

We have shown that the current patterns of variation in chick coloration correlate with a parental strategy to optimize food allocation within families: Hatching asynchrony, followed by brood division and parental favoritism of the smallest most colorful chicks that remain after a period of scramble competition and brood reduction (35). However, these patterns do not necessarily explain why American coot chicks show such extreme ornamentation compared to many other close relatives (13). One or more other factors could have feasibly contributed to the evolutionary elaboration of juvenile ornaments. For example, we studied only a subset of the many ornaments that coot chicks have, that include both static and dynamic signals, and it seems unlikely that each of these different ornaments evolved completely independently of each other. Selection for parents to attend to some ornaments could have favored the evolution of parental preference patterns that then set the stage for other ornaments that mimic or amplify the original trait that selects for parental preference (32). Second, Kilner (14) suggested that current patterns of variation in chick signals may reflect the resolution of past evolutionary conflicts within families. In the case of American coot chicks, current levels of ornamentation could reflect the resolution of conflicts both within and between families (i.e., conspecific brood parasitism). Finally, these factors could work in conjunction with purely social factors, whereby factors that initially favor parental preference potential create the conditions for runaway social selection that would exaggerate the trait well beyond levels favored parental preference in the first place (4, 48). One way to resolve these outstanding questions would be to leverage the natural variation in juvenile ornamentation within this family of birds [Rallidae (13)] to conduct comparative studies of the relation between chick coloration, parental favoritism, and brood parasitism.