Invited commentary on 'intersexual social dominance mimicry drives female hummingbird polymorphism'

In a new study, Falk et al. [1] examine the white-necked Jacobin (Florisuga mellivora). This hummingbird is unique among hummingbirds in that it has female polymorphism [2]. Females come in two distinctive morphs: in the Panamanian population they studied, roughly 80% of females are dull-plumaged and dissimilar to males, while 20% of females have the same bright plumage of males, making them indistinguishable from males visually [3], although slight dimorphism in morphology permits identification of females in the hand. Moreover, juvenile birds of both sexes (i.e. those in their natal plumage) more closely resemble the bright plumage of adult males than the dull plumage of females. White-necked Jacobin seems completely unique in this respect: in all other dimorphic bird species, juvenile birds more closely resemble adult females.

Sex-limited polymorphism is a special case of sexual dimorphism. Why does sexual dimorphism evolve? Darwin and Wallace debated the cause in birds: Darwin invoked female aesthetic preferences to explain why males were brightly coloured (i.e. sexual selection), while Wallace emphasized natural selection for camouflage on an exposed nest to explain why females were more cryptic [4].

Dimorphism is most prevalent in species in which the sexes differ in how much they invest in producing offspring. For instance, Wallace's hypothesis applies to species where the female does all the work, not species where both sexes incubate. In birds, roughly 90% of species are socially monogamous, where both parents make substantial (although not necessarily equal) investment in offspring. Of the remaining 10% that are not monogamous, hummingbirds, a large clade of roughly 350 species, are fully one-third of the total. Remarkably, in not a single species are males known to help care for offspring. That is, there are no credible reports of males incubating, and no credible reports of a male provisioning either the offspring or their mother with food. But that said, for such a large clade, their mating systems are surprisingly poorly characterized (there seem to be more studies of mating systems of the 54 species of manakins (Pipridae) than of the 350 hummingbirds). While many hummingbird species apparently lek [5], in others males guard female nesting areas, or appear to engage in resource defence polygyny [6]. In at least a few species, females do not nest on male territories and males selectively allow certain females to feed from flowers on his territory [7], while guarding the territory from other hummingbirds, especially rival males.

So how does female polymorphism fit in? It is not yet entirely clear. Polymorphism is fascinating because it requires special conditions, such as negative frequency-dependent selection (i.e. as one morph becomes rarer, it performs better) to maintain both morphs at the same time in the same population. Otherwise selection will tend to remove the less-fit morph. Most instances of polymorphism in birds are exhibited by both sexes [8]. Polymorphism may be limited to one sex when it relates to life-history strategies that pertain to one sex only. Why would polymorphism be limited to females? In their new study, Falk and colleagues consider two hypotheses: are male-like females deceptive mimics, evading aggression because they visually mimic (but don't act) like males? Or do the male-like females also have other male-like attributes, such as differences in flight ability and the behaviour of guarding a nectar source, thus acting like males as well (a 'male behaviour' hypothesis)? Based on a standardized flight test and the spatial use of hummingbird feeders by RFID-tagged birds in the wild, they support the former hypothesis: male-like females behaviourally resemble the female-like females and do not seem to have resource-holding potential of males. The rejection of the male behaviour hypothesis is unsurprising for an additional reason not explored by Falk and colleagues: flower-guarding by female hummingbirds is rare because guarding a patch of flowers entails trade-offs with the other thing females do: they nest.

Nesting hummingbirds are subtle and surreptitious. Thus, most studies of hummingbird mating systems have focused disproportionately on males. We have limited data on what nesting females must do. Daily nectar consumption of a captive hummingbird over the duration of a successful nesting bout is shown in figure 1. Although hummingbirds are famous for drinking nectar as their main source of calories, newly hatched chicks double their mass a few times over the first week [9]. To grow rapidly they at first mainly require protein, not sugar (figure 1). The females get this protein by foraging extensively on insects and spiders [10]. This seems to be why females of some species tend to place their nest in the vicinity of areas with plentiful arthropods, such as streams [11], rather than near flowers. As the nestlings approach fledging, they then consume more nectar, and the female's daily nectar requirements rises to nearly triple her baseline nectar consumption (figure 1).

Figure 1.

Nectar consumption by a captive Costa's hummingbird (Calypte costae) during a successful nesting attempt in an outdoor aviary. Arthropods (mainly Drosophila) were available ad lib.; her consumption of them was not quantified. Each millilitre of nectar contained 0.1 g of complete hummingbird diet, Nektar-Plus (Nekton GmbH, Dammfeld, Germany). Female mass: roughly 3.2 g. Offspring reached 3.8 g because they were hybrid C. costae x C. anna. (Online version in colour.)

Despite having high need for nectar, especially near the end of nesting, the female has little ability to guard flowers. Guarding flowers requires near-constant vigilance, but she is busy with other essential behaviours such as nest-building, incubating or flycatching. Guards vocalize and make themselves obvious to intruders, which is counterproductive to the goal of concealing the location of a nest. Incidentally, as females of some species can rapidly re-nest days after the previous chicks fledge, her period of elevated nectar intake (figure 1) might coincide with preparations for her next breeding attempt, which includes deciding on a mate. Males hoping to influence her decision might do so by guarding the best nectar sources.

Falk and colleagues have not yet fully established the frequency-dependent mechanism that permits both morphs to coexist. As they mention, many biological questions about females remain under-studied. That is true of this species as well. Measuring nesting success of the morphs would permit a powerful within-species test of the Wallace–Darwin debate, as Wallace predicts that nests of bright females fail due to predators more often (and such predation could easily be frequency-dependent). Another obvious question is how courtship and copulation actually works. The previous finding that males attack the female-like females more than the male-like females [3] leaves this unanswered. Maybe males attack unfamiliar females [3], but when a familiar female is preparing to breed, the males instead selectively court and permit her to feed, similar to what another hummingbird, purple-throated carib, does [7]. There remain many open questions about what maintains polymorphism in this species.

More generally, female polymorphism is under-studied. Male polymorphism occurs in many animal taxa, in association with alternative strategies of mate acquisition [8], such as ruffs (Calidris pugnax), in which the polymorphism is well studied. But actually, in birds, female polymorphism may be more common than male polymorphism: a review reported only two birds with male polymorphism, while 23 with female polymorphism [8]. Most of these 23 are cuckoos, which are nest parasites: the female morphs mimic different predators such as hawks or kestrels, which are hypothesized to permit the rarer morph to more easily gain access to host nests [12]. Females are under-studied: there are more papers on the male polymorphism in the ruff than on the female polymorphism in various species of cuckoos.

Are there more examples of female polymorphism within hummingbirds? Possibly, but in each case alternative explanations for the limited existing data have not yet been ruled out. Two species in the hummingbird genus Anthracothorax have reports of male-plumaged females laying or sitting on eggs [13]. But these ‘morphs’ seem rare. Perhaps it is age-related: they moulted into male plumage in old age as hormone levels decline, as can happen in certain other bird clades such as Galliformes. There are also reports of female polymorphism from the genus Heliangelus [14]. As the inference came from museum specimens spanning many geographical localities, and this genus is highly geographically variable, verifying that there are multiple female types from the same population is needed. The dearth of records of male-plumaged birds attending a nest suggests female plumage polymorphism is rare in hummingbirds [15], since male-plumaged females would, at first pass, be mistaken for an actual male. The discovery of any hummingbird species in which male-plumaged birds (whether actually male or female) attended a nest would be highly interesting for further study.

Ethics

Data shown in figure 1 were collected under permits from USFWS, CDFW and with approval from the IACUC at UC Riverside.

Data accessibility

All data are shown in the figure.

Conflict of interest declaration

I declare I have no competing interests.

Funding

I received no funding for this study.