Sex matters in the race to combat climate change

This blog post is provided by Rachael Y. Dudaniec, Alexander R. Carey, Erik I. Sve­­nsson, Bengt Hansson, Chuan Ji Yong and Lesley T. Lancaster and tells the #StoryBehindThePaper for the paper ‘Latitudinal clines in sexual selection, sexual size dimorphism, and sex‐specific genetic dispersal during a poleward range expansion’, which was recently published in the Journal of Animal Ecology.

As climate change is facilitating many species to expand their ranges into novel areas, one may wonder if males and females are responding in the same way, and if these massive disruptions are creating new interactions, or possibly, altercations, between the sexes as they battle their way through foreign territories. It is possible that sex-differences in behaviour, appearance or physiology along a range expansion gradient may affect how successful individuals are at adapting to novel environmental conditions. This can lead to variation in how different sexes become distributed across space, and how they adapt to their environments. This phenomenon of ‘spatial sorting’ of individuals that possess favourable traits can therefore affect the rates of range expansion, but little is known about how sex differences in these traits impacts such expansions.

In insects, males and females of the same species may differ in body shape, size or colour, or levels of environmental plasticity in traits that impact dispersal and reproduction. Here, we investigate how sex differences in morphology, behaviour and genomic population differentiation may impact the climate-mediated poleward range expansion of the common bluetail damselfly (Ischnura elegans) in northern Europe. We sampled 65 sites along a 583 km gradient including the expanding I. elegans range margin in Sweden, and quantified gradients in local abundance, sex ratio and sex-specific shifts in body size and mating status. Mating status was measured via the ‘copulation status’ of the damselfly, which was either solitary and unpaired, or paired, with males and females captured in the ‘mating wheel’ formation, which forms a distinctive love heart shape (see picture).  

The characteristic love heart shaped ‘mating wheel’ formation of Ischnura elegans. Photo by Rachael Dudaniec

In many insects, including I. elegans, females are conspicuously larger than males, however towards the cooler, northern range limit, male damselflies had a larger body size than in the range core, a trait that is advantageous for dispersal capacity. This increase in size was not reflected in females, resulting in relaxation of sexual size dimorphism at the expanding range edge. The reasons for the lack of change in female body size is not known, but may indicate a lack of selection for a larger, dispersal-enhancing female body size due to existing behavioural or morphological constraints.

There was also a male-biased sex ratio towards the range limit. Despite this, these larger, northern males were less likely to be found in copula with females compared to their smaller counterparts. This observation was striking given that the reverse pattern occurs in the south of the I. elegans range, where larger males are under sexual selection. These findings suggest that sexual selection is not an important driver of this increased size, but rather, effects of the climate-driven range expansion on natural selection, shaping its male passengers for a speedy journey at the expense of having less success with the opposite sex.

Complementing this field data with genetic information for 426 individuals from 25 sites, we could further see how the sexes differed in gene flow and migration rates. These data indicated that males were more likely to migrate north, and for longer distances, than females. Sex-specific differences in dispersal were also revealed by investigating how genetically similar individuals of the same sex were to each other at different spatial scales. This test showed us that females are more ‘sedentary’ as they stay more genetically similar to each other at shorter distances than do males.

When investigating how landscape and climatic features can limit or facilitate sex-specific genetic connectivity along the expansion gradient, we found that annual temperature had a strong linear effect on genetic dispersal. This temperature effect was consistent across both sexes, and in all cases an effect of landcover features on genetic dispersal (such as vegetation cover and roads) was entirely absent. Within the cooler temperatures towards the northern range edge, it was harder for gene flow to occur, representing another challenge for larger males moving longer distances as they reach their new, colder, northern frontiers.

Altogether, we present a story of male-biased, longer distance dispersal during range expansion combined with limited mating success of larger, northern males. These northern males also encountered lower temperatures that are more difficult to disperse through and provide high resistance to gene flow. These findings have emergent consequences for the evolution of the sexes and sex differences in population structure in I. elegans during range expansion. While males are more likely to colonise novel areas ahead of females in I. elegans, which is so far, exhibiting a successful range expansion in Sweden, adapting to a rapidly changing climate is not without disruption to sex-specific interactions, which may ultimately play a key role in the success of future population persistence.

Evolution of dance and color in the birds of paradise

In this post, we take a behind-the-scenes look at a recent study into the drivers of complexity in bird of paradise displays. Meredith Miles, a PhD student in Dr Matthew Fuxjager’s lab at Wake Forest University, takes an integrative approach into behavioural ecology. This involves studying the molecular and physiological mechanisms that underlie display performance all the way up to the diversity of macroevolutionary pattern generated by sexual selection for displays.

Birds of paradise—the gaudy songbirds known for their bizarre courtship displays and ornamental plumage—evolved from a crow-like ancestor as early as 24 million years ago. These large and charismatic birds boast both cultural and scientific significance; indigenous peoples and 16th century Europeans alike considered them to be “Birds of God” or mythical phoenixes, and the birds’ elaborate courtship routines have inspired figures from Alfred R. Wallace to Sir David Attenborough. Indeed, this island-endemic lineage serves as a prime example for how sexual selection drives the evolution of extraordinary behavior. Birds of paradise also offer a unique opportunity to leverage the phenotypic complexity of their displays to uncover hidden truths about the process of evolution.

BoP merged

There are over 30 bird of paradise species, each with its own unique visual display. These encompass both color and gesture, and have evolved due to intense sexual selection by female choice. Left: male Raggiana bird of paradise (Paradisea raggiana). Right: male and female Wilson’s birds of paradise (Diphyllodes respublica). Photos: Dr. Marcel Holyoak.

How can we study something as complicated as animal dance and “costume”? At its core, dance is simply an extreme example of a gestural display, or body movement used for communication. The gestural complexity of a given species’ display simply refers to the number of unique movements incorporated into the whole routine. Over the years, diligent naturalists have compiled extensive (and evocative) descriptions of gestural displays, which we used to tally up a gestural complexity score for each species. For example, consider the following description of the king bird of paradise’s Dancing Display:

“… In this display he fluffs out his plumage, squats low to the perch, spreads the pectoral fans high, and cocks the tail so steeply that the wires are tilted forwards reaching above and beyond his head” – Frith and Beehler, 1998.

In this single posture alone, there are four unique movements: the bird (1) crouches down, (2) raises its tail, (3) spreads the specialized breast plumes, and (4) erects the rest of the body plumage. These are common elements we see in the displays of many other species too, and we thus award the species a point in the corresponding gestures. Combing through pages of similar accounts gives us an exhaustive look at each species’ behavior, and ultimately lets us generate a quantitative index of gestural complexity for all birds of paradise.

KingBopFigure

At first glance, this portion of a king bird of paradise’s Dance Display might look like a single movement—but it actually consists of multiple component gestures that are shared with many other species. Only by breaking down gestural displays into these “raw ingredients” can we begin to understand how animal dance evolves.

What drives the evolution of complex dance routines? These gestures are the key to courtship for birds of paradise, but we found that only display habitat—rather than indices of sexual selection—predicts the macroevolutionary pattern: species that display in the dense forest understory use more gestures than their canopy-displaying counterparts. This may be because display habitat profoundly affects how well a signal can be transmitted to the receiver. Displaying in the “visually cluttered” understory might increase the pressure for males to evolve more visible displays, and one way to accomplish this is through adding more gestures to the dance.

We can also characterize color ornaments by scoring how much male plumage has diverged from its female counterpart. This works thanks to an ancestral state reconstruction of sexual dimorphism, which shows us that birds of paradise descended from an ancestor in which both males and females were drab. Unlike dance complexity, color is not associated with display habitat on a macroevolutionary scale. Instead, males appear to become more colorful in response to the adoption of a lek mating system (which is characterized by extreme sexual selection by female choice). We can even break down our investigation of color to distinguish between melanin-based (blacks, browns, and other “earthtones”) and carotenoid-based (red and yellow) ornaments. Although pigment basis for colors does not change with species display habitat or mating system, it does appear to be influenced by male sociality: species in which males gather together and directly compete at a single display ground trade in melanin colors for bright carotenoid ornaments instead. Together, this suggests that males undergoing a higher relative degree of sexual selection by female choice—as reflected in the lek mating system—will evolve to be more colorful overall. However, increasing pressure of male-male competition appears to specifically influence the evolution of bright red and yellow color patches.

graphicsabs

 Four representative species illustrating the main evolutionary trends we uncover in the study. Different selection pressures are each associated with shifts in a specific display trait.

Altogether, our results suggest that these complex displays exhibit modular evolution: each component of the display (e.g., gesture or color) acts as a distinct “module” that undergoes an independent evolutionary trajectory. Modular displays may be evolutionarily significant because they allow for multiple—and potentially opposing—selection pressures to simultaneously act on the same display without impeding one another.

Of course, a female bird of paradise evaluating a male’s display is probably not scoring his choreography and color. Instead, an animal must perceive the display in its entirety, which encompasses auditory and tactile signals as well as visual. And within the visual display itself, gesture is even used to show off specific color ornaments. In this way, modular evolution allows the integrated display’s complexity to be multiplicative rather than additive: its attractiveness to the receiver is more than the sum of its modular parts.  However, it is only by examining these parts individually that we can understand what drives their independent evolution.

More Info:

Miles, M.C. and Fuxjager, M.J. (in press). Synergistic selection regimens drive the evolution of display complexity in birds of paradise. Journal of Animal Ecology.

Competitive males are a blessing and a curse

jae-2016-00123-r2-2This post is a press release from the authors of Journal of Animal Ecology paper “Sexual selection can both increase and decrease extinction probability: reconciling demographic and evolutionary factors” by Carlos Martínez-Ruiz and Robert J. Knell Issued by Queen Mary, University of London Press Office.

Showy ornaments used by the male of the species in competition for mates, such as the long tail of a peacock or shaggy mane of a lion, could indicate a species’ risk of decline in a changing climate, according to a new study from Queen Mary University of London (QMUL). Continue reading