Sexual Dimorphism and Floral Polymorphism in a Hummingbird-Plant Association
Sexual dimorphism in size and morphology is widespread in the animal kingdom. Charles Darwin drew attention to these differences, and offered three explanations for their evolution based on mechanisms of sexual selection, fecundity selection, and ecological causation, e.g., resource- partitioning. Although empirical studies demonstrate that the first two mechanisms operate in natural populations, unambiguous examples of ecological causation of sexual dimorphism have been hard to find, because in many animal species, sexual differences in the size of feeding structures scale positively with body size. The positive relationship between body size and feeding morphology makes it unclear whether ecological differences between the sexes are the cause or the consequence of sexual dimorphism.
Since 1999, I have been studying sexual dimorphism in the purple-throated carib (Eulampis jugularis) on the island of St. Lucia, West Indies. Although the wings and body masses of males average 8.6% and 25% larger than those of females, the bills of females average 20% longer and 40% than those more curve than those of males, one of the most extreme bill dimorphisms of any hummingbird.(See picture.)
In studies with Amherst students Irvin Pan [‘99], Jill Brennan [‘01], and Jed Horwitt [‘01], I found that the purple-throated carib is the sole pollinator of two species of Heliconia, a red-bracted H. caribaea, and a green-bracted race of H. bihai endemic to St. Lucia. Flowers of H. caribaea correspond in size and shape to the bills of male caribs, whereas flowers of the green-bracted H. bihai correspond in size and shape to the bills of female caribs. Further evidence for ecological causation of sexual dimorphism (and plant-pollinator coevolution) was provided by a geographic replacement of H. caribaea by H. bihai where the former is rare, and the subsequent development of a floral dimorphism in H. bihai, with a red-green bracted morph with flowers matching the bills of males, and a green-bracted morph with flowers matching the bills of females (see 2000. Science 289:441-443 PDF ). (See picture.)
More recently, John Kress, Curator of Botany at the Smithsonian Institution and a leading authority on Heliconia taxonomy and systematics, and I found additional support for ecological causation of sexual dimorphism in the purple-throated carib from studies on the island of Dominica, 120 kilometers to the north. As on St. Lucia, Dominica has both H. caribaea and H. bihai, with flowers of the former matching bills of males and flowers of the latter matching bills of females. But on Dominica, H. bihai has only one more, which is red with a yellow stripe (See picture.) H. caribaea is more common than H. bihai, and it is the Heliconia species with two color morphs: a yellow-bracted morph with shorter, straighter flowers matching the bills of males, and a red-bracted morph with longer, more curved flowers matching the bills of females. Not only that, but the replacement morphs on Dominica or St. Lucia either reduce (Dominica) or increase (St. Lucia) their nectar reward through decreases or increases in their numbers of bracts and flowers in correspondence to the size and energy requirements of their female or male pollinator. This latter finding suggests that sexual differences in body size of purple-throated caribs, and not just their bill morphology, are maintained by feeding specialization on the different Heliconia food plants (Temeles and Kress. 2003. Science 300:630-633 PDF ).
The roles of food and sex in Heliconia use by purple-throated caribsBoth intersexual food competition and sexual selection may result in male-male competition for territories, either as food sources during the non-breeding period, or as feeding-and-mating territories during the breeding period. Competition between males and females for flowers during the non-breeding season is an unambiguous indicator of intersexual food competition. Because many females that intrude onto male territories during breeding periods copulate with males, however, it is unclear whether male territorial defense during the breeding period is mostly for food, and driven by intersexual food competition, or is mostly for sex, and driven by sexual selection.
To discriminate between these two alternatives for territory maintenance, my students and I experimentally reduced flower numbers on territories of four different males by covering Heliconia flowers with clear plastic bags on male territories in 2000, 2001, and 2002 on the island of St. Lucia. If breeding territories are defended primarily for sex, then experimental reductions of flower numbers on male territories should have little effect on the amount of time a male spends on the territory. This was why we covered bracts with clear bags: if breeding territories are for sex, then clear plastic bags should not reduce territory attractiveness if inflorescences (flower stalks) are a signal of male quality. Alternatively, if breeding territories are defended primarily for food, we expected males to spend more time off of territories feeding following experimental reductions of flower numbers on their territories, as well as lose weight, which we monitored by weighing males with electronic balances fitted to Heliconia inflorescences (See picture.)
Following inflorescence reductions, males reduced the time they spent feeding on their territories and lost a significant amount of weight, but increased their time feeding and regained weight to pre-manipulation levels following restoration of flower abundance. Territorial males also reduced the amount of time they spent in defense and in mating chases following inflorescence reductions. Both results indicate that males derive an energy benefit from defense of Heliconia territories during the breeding season, in contrast to studies of some other hummingbird species. In all three years, significantly more females intruded onto the more rewarding H. caribaea than onto H. bihai territories, suggesting that the quality of a male’s territory may be a cue for female choice of mates in this hummingbird-flower system (This research was published in the Condor 2004, volume 106:691-695).
Sexual dimorphism and foraging and territorial economics at three heliconias
Additional support for the role of food in driving this hummingbird – Heliconia system comes from a study of foraging and territorial economics at the three heliconias on St. Lucia. Across three years of study, H. caribaea territories defended by males were significantly smaller in area and had higher densities of flowers than red-green H. bihai territories, and both kinds of male Heliconia territories were smaller and had higher densities of flowers than a green H. bihai territory maintained by a female (females were rarely observed on Heliconia territories and the single female post-breeding territory was the only female territory found in three years’ of studies). My undergraduate students and I used measured metabolic costs of sleeping, resting, and hovering for purple-throated caribs obtained by Wolf and Hainsworth (1971 Ecology), and Gill’s and Wolf’s (1975 Ecology) equations for territory and foraging economics of sunbirds (modified for the hummingbirds), to estimate the relative costs of foraging and defense for male and female purple-throated caribs at the three heliconias. The smaller territory areas and higher flower densities of H. caribaea territories lowered males’ foraging time and energy costs per flower relative to red-green H. bihai territories, which theoretically allowed them to meet their energy demands in less time and at lower cost. Males’ estimated foraging time and energy costs were greatest at the green morph of H. bihai, and compared to females, they would save a higher proportion of time and energy by foraging at H. caribaea and the red-green morph of H. bihai. (See figure.)This asymmetry in relative gains from foraging at each of the three heliconias for males and females may further reinforce resource partitioning between them, in addition to differences in size and fighting abilities (This research was published in the Auk 2005, volume 122:187-204).
Feeding performance and bill morphology of the sexes
As noted above, sexes of purple-throated carib hummingbirds exhibit extreme sexual dimorphism in bill morphology, with males having short, straight bills and females having bills 20% longer and 40% more curved. We have been analyzing feeding performance of males and females in order to understand how these differences in bill morphology between the sexes contribute to niche partitioning. These experiments involve the use of natural Heliconia flowers on St. Lucia and 34 artificial flowers differing in length, curvature, and diameter. The use of artificial flowers allows us to examine birds’ feeding performance at floral phenotypes not found in nature, and gives us insight into how their bills would respond to selection were there environment to change.
Our most exciting finding to date is evidence for a trade-off in the relative advantages of short, straight bills and long, curved bills. Specifically, the longer, more highly curved bills of female purple-throated caribs allow them to feed from longer, more highly curved flowers than males, and to do so more quickly, when the birds perch on Heliconia bracts to feed (See figure). Males had great difficulty extracting nectar from flowers of the green morph of H. bihai, and in many cases could not insert their bills into flowers of the green morph due to mismatches between bill and flower shape (seevideo clip).
Experiments with artificial flowers supported those with real Heliconia flowers. Only 1 of 6 males was able to extract nectar from an artificial flower of dimensions 44 mm long x 3 mm wide x 0.04 1/mm curvature, replicating the dimensions of the green morph of H. bihai on St. Lucia visited primarily by females. In contrast, even though the bills of males are much shorter than the bills of females, they could extract nectar from the same maximum length of straight flowers while hovering Moreover, males had significantly faster handling times and better feeding performance than females when hovering to feed from perfectly straight flowers (See figure). See Temeles et al. 2009 Ecology.
Mate choice and mate competition in a tropical hummingbird
In addition to examining feeding performance of male and female purple-throats in the context of natural selection, we examined sexual selection acting on males. Our earlier studies demonstrated a close correspondence between energy rewards of the heliconias and the body size and energy needs of sexes of purple-throats and suggested that natural selection may have had a role in the evolution of body sizes of the sexes (Temeles et al. 2000, 2005; Temeles & Kress 2003). Because male purple-throats also defend heliconias for breeding, however, we noted that sexual selection may have had a role in the evolution of their larger size. In a study of a population of 12 males defending territories of H. caribaea on the island of Dominica, we found that males defended territories greatly in excess of their energy needs, and that females preferred to mate with males having the highest standing crops of nectar on their territories (Temeles & Kress 2010). Males specifically maintained plants on their territories for use by females, a behavior we have termed “flower farming” (See figure). A male’s ability to accumulate high standing crops of nectar on his territory depended on his ability to evict intruders, as well as on his size, with larger males being the most successful. Thus, sexual selection contributes to the larger size of male purple-throated caribs.
Sexual dimorphism in hermit hummingbirds
The purple-throated carib hummingbird and its Heliconia food plants provide some of the best evidence to date for ecological causation of sexual dimorphism, but also raise the question of whether this evidence is simply an isolated case resulting from ecological release on islands or alternatively is more widespread than previously imagined. The purple-throated carib is absent from the islands of Grenada, Tobago, and Trinidad, even though one of the heliconias it visits, H. bihai, occurs there. Another aspect of our work is to determine what hummingbird(s) replace purple-throats geographically as pollinators of H. bihai (and H. caribaea). Heliconia bihai, on these three islands is a generalist with extremely short flowers pollinated by 3 to 6 hummingbird species per island. We discovered that two of these hummingbirds, the rufous-breasted hermit, Glaucis hirsutus, and the green hermit, Phaethornis guy, have sexual dimorphism in bill curvature similar to that of the purple-throated carib. This discovery prompted a phylogenetic analysis of sexual dimorphism within the hermit hummingbirds (Phaethornithinae) in which we determined that sexual dimorphism in bill curvature is widespread within this subfamily (See figure). Moreover, our own field observations together with those of Taylor and White indicate that the sort of sexual partitioning of heliconias we have documented for purple-throats also occurs in many species of hermit hummingbirds, and that ecological causation of sexual dimorphism may be more common than has been previously thought. (See figure). See Temeles et al. 2010 Philosophical Transactions of the Royal Society B.
Pollinator-mediated selection on Heliconia floral traits
The close correspondence betweeen the bills, body sizes, and energy requirements of male and female purple-throated caribs to the corolla lengths, bract numbers, and energy rewards of their Heliconia food plants suggest that the birds have had a major role in the evolution of floral traits in H. bihai and H. caribaea. We evaluated the strength and direction of natural selection on corolla length and number of bracts per inflorescence in allopatric populations of H. bihai and H. caribaea for five populations on the island of Dominica, West Indies, over a two-year period by relating seed production to floral traits (see Temeles et al. 2013). In H. bihai, directional selection for longer corollas was always significant with the exception of one population in one year, whereas selection on bract numbers was rare and found only in one population in one year (see figure). In contrast, significant directional selection for more bracts per inflorescence occurred in all three populations of the yellow morph and in two populations of the red morph of H. caribaea, whereas significant direction selection on corolla length occurred in only one population of the red morph and one population of the yellow morph (see figure). Selection for longer corollas in H. bihai may result from better mechanical fit, and hence pollination, by the long bills of female purple-throated caribs, the sole pollinator of H. bihai on Dominica. In contrast, competition between male purple-throated caribs for the most rewarding territories may drive selection for more bracts in H. caribaea. Competitive exclusion of female purple-throated caribs by males also implicates pollinator competition as a possible mechanisms for floral divergence in the two heliconias and their morphs, which we are currently investigating through experiments in our enclosed Heliconia garden on Dominica (see figure). .
Pollinator competition as a driver of floral divergence
Optimal foraging models of floral divergence predict that competition between two different types of pollinators will result in partitioning, increased assortative mating, and divergence of two floral phenotypes. We tested these predictions in a tropical plant-pollinator system using sexes of purple-throated carib hummingbirds (Anthracothorax jugularis) as the pollinators, red and yellow inflorescence morphs of Heliconia caribaea as the plants, and fluorescent dyes as pollen analogs in an enclosed outdoor garden. When foraging alone, males exhibited a significant preference for the yellow morph of H. caribaea, whereas females exhibited no preference. In competition, males maintained their preference for the yellow morph and through aggression caused females to over-visit the red morph, resulting in resource partitioning. Competition significantly increased within-morph dye transfer (assortative mating) relative to non-competitive environments. Competition and partitioning of color morphs by sexes of purple-throated caribs also resulted in selection for floral divergence as measured by dye deposition on stigmas. Red and yellow morphs did not differ significantly in dye deposition in the competition trials, but differences in dye deposition and preferences for morphs when sexes of purple-throated caribs foraged alone implied fixation of one or the other color morph in the absence of competition. Competition also resulted in selection for divergence in corolla length, with the red morph experiencing directional selection for longer corollas and the yellow morph experiencing stabilizing selection on corolla length. Our results thus support predictions of foraging models of floral divergence and indicate that pollinator competition is a viable mechanism for divergence in floral traits of plants (see Temeles et al. 2016 PLoS One.