Evolution Highlight: Differential introgression of a female competitive trait

Each month, the Evolution Highlights series will highlight some of the interesting and varied papers published within the last few years in Evolution. The goal of these Evolution Highlights is to let our readers learn more about how the highlighted study came into existence, and to invite the authors to share stories and tips from the perspective of a recently published author. We welcome nominations and self-nominations for the Evolution Highlights. Find out how to submit a paper here.

Differential introgression of a female competitive trait in a hybrid zone between role-reversed species
Sara E. Lipshutz, Joana I. Meier, Graham E. Derryberry, Matthew J. Miller, Ole Seehausen, Elizabeth P. Derryberry

https://onlinelibrary.wiley.com/doi/abs/10.1111/evo.13675

Abstract:
Mating behavior between recently diverged species in secondary contact can impede or promote reproductive isolation. Traditionally, researchers focus on the importance of female mate choice and male–male competition in maintaining or eroding species barriers. Although female–female competition is widespread, little is known about its role in the speciation process. Here, we investigate a case of interspecific female competition and its influence on patterns of phenotypic and genetic introgression between species. We examine a hybrid zone between sex‐role reversed, Neotropical shorebird species, the northern jacana (Jacana spinosa) and wattled jacana (J. jacana), in which female–female competition is a major determinant of reproductive success. Previous work found that females of the more aggressive and larger species, J. spinosa, disproportionately mother hybrid offspring, potentially by monopolizing breeding territories in sympatry with J. jacana. We find a cline shift of female body mass relative to the genetic center of the hybrid zone, consistent with asymmetric introgression of this competitive trait. We suggest that divergence in sexual characteristics between sex‐role reversed females can influence patterns of gene flow upon secondary contact, similar to males in systems with more typical sex roles.

Evolution Highlight by Sara Lipshutz
Biology - Ecology, Evolution, Behavior, Indiana University

What gave you the idea for this study?

I’ve been fascinated by jacanas since I learned about their mating system as an undergraduate – they were on the cover of my Animal Behavior textbook. Most jacana species are sex-role reversed, meaning that in comparison to males, sexual selection is stronger on females to compete over mating opportunities. Females are polyandrous and mate with multiple males who conduct all parental care. When I learned from my coauthor Matt Miller that two Neotropical species, Northern jacanas and wattled jacanas, interbreed in Panama, I wondered how interspecific female competition might influence patterns of hybridization.

In what ways does this study expand or build on your previous studies?

We had previously characterized the jacana hybrid zone based on mtDNA and two nuclear loci, as well as plumage and facial ornamentation (Miller et al. 2014, BMC Evolutionary Biology). We found that phenotypic hybrids had northern jacana mtDNA more often than expected, suggesting that northern jacana females disproportionately mother hybrid offspring. We assessed potential differences in competitive traits of the two species and found that female northern jacanas had larger body mass, longer wing spurs, and were more aggressive in response to a simulated territorial intrusion than wattled jacana females (Lipshutz 2017, Behavioral Ecology and Sociobiology). This study in Evolution expands on past work by using thousands of genome-wide loci to estimate the center and width of the jacana hybrid zone, as well as examining clinal transitions in competitive traits – wing spur length and body mass. The reproductive success of female jacanas depends on their ability to defend and maintain breeding territories, so we predicted that divergence in competitive traits between the species could influence introgression patterns.

From your perspective, what was the most interesting or intriguing aspect of this study?

By characterizing patterns of genetic and phenotypic introgression between northern and wattled jacanas, we found that the transition in female body mass is displaced relative to the genetic transition between the species. This is consistent with asymmetric introgression of this competitive trait, from the larger northern jacana into the smaller wattled jacana across the hybrid zone. These patterns align with findings from other hybrid zones in which male-male competition explains asymmetric introgression from the more dominant species into the less dominant species. Whereas previous work on sexual selection and speciation predicts that females are the gatekeepers of species barriers, we find that divergence in sexual characteristics between sex-role reversed females can influence patterns of gene flow upon secondary contact, similar to males in systems with more typical sex roles.

Were there any unexpected logistical or technical challenges you had to address?

Catching jacanas with mist nets is challenging, given that they live on top of floating vegetation or in flooded areas. We got creative with our strategies, relying on kayaks and the generosity of Panamanian farmers, who sometimes gave us tractor or horse rides on their land. This work was made possible by several amazing field teams, consisting of colleagues from the Smithsonian Tropical Research Institute, students from the University of Panama and Tulane University, and assistants from the United States and the United Kingdom (see photo of field assistants).

Did your work take you to any interesting locations? If so, what were they like?

We sampled parental population of both species outside the hybrid zone as well as heavily in the hybrid zone, so we traveled from Palo Verde, Costa Rica to east of the Panama Canal. Some field sites had deep water with crocodiles, others were cattle, pig, or rice farms, and others were wetlands with thick mud (see boot rescue in bottom right photo of field assistants).

Tell us something about collecting these data that people might not know or think about.

There’s sometimes an expectation that research with wild animals is being done in pristine habitats, but the majority of localities where we study jacanas are agricultural landscapes.

Do you have any writing tips for others?

This study was meant to be my first chapter, but it took all of my PhD to complete. My advice for others is something I learned as a graduate student in New Orleans during Mardi Gras: it’s a marathon, not a sprint. It’s important to have structured goals for each stage of data collection, from fieldwork to lab work to analysis and writing, and it’s also important to build in more time than you think you’ll need. Weekly writing workshops in the Derryberry Lab helped me stay on track, and I received invaluable feedback from my mentors and peers at lab meetings, conferences, and visiting seminars. Presenting my work informally and formally helps me improve how I contextualize my results and their implications, all of which clarify my writing. Be kind to yourself, be patient with your progress, and seek feedback from others.

Was this study collaborative with other groups? If so, what was valuable about that experience?

I’ve been really fortunate to collaborate with my coauthors, who have been my mentors at various stages before and during my doctoral dissertation (see photo, right). Matt Miller hired me as an intern at the Smithsonian Tropical Research Institute in Panama when I was fresh out of undergrad. My PhD advisor Elizabeth Derryberry put a lot of trust in me to pursue this system and supported me at every stage. Ole Seehausen generously hosted me as an NSF GROW fellow in Switzerland, where Joana Meier helped me improve my understanding of population genomic analyses. I also benefited immensely from working with Graham Derryberry, who wrote the R package HZAR, to fit molecular and morphological data from the hybrid zone to cline models.

Looking back, what is one thing you learned from doing this study (other than your main findings) that you’ll use in future projects?

I love combining muddy boots fieldwork with molecular techniques, and I’m excited to continue integrating these two approaches in my ongoing work on this system.

Sara Lipshutz

Top: Northern Jacana (Jacana spinosa). Note yellow, tri-lobate frontal shield and chestnut-brown plumage.
Bottom left: Northern x Wattled Jacana hybrid. Note yellow frontal shield with reduced wattles.
Bottom right: Wattled Jacana (Jacana jacana). Note red, bi-lobate frontal shield, red hanging wattles, and black plumage.

Field assistants

Top row from left: Sara Lipshutz, Joana I. Meier, and Graham E. Derryberry
Bottom row from left: Matthew J. Miller, Ole Seehausen, and Elizabeth P. Derryberry