Differences between males and females affect patterns of evolutionary diversification

Published in Ecology & Evolution
Differences between males and females affect patterns of evolutionary diversification
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How do differences between the sexes affect evolutionary diversification? Considering that males and females of the same species share the majority of the genome and typically inhabit the same environments, it is often assumed that trait evolution in the two sexes largely occurs in parallel. But members of each sex fundamentally differ in the ways they can maximize their fitness, with males exhibiting adaptations to secure mating opportunities and females exhibiting traits that facilitate the production of offspring. How sexual selection on males and reproductive constraints on females affect broad scale patterns of trait evolution and species diversification remains understudied. 

We investigated this problem in live-bearing fishes of the family Poeciliidae. Unlike many other fishes, females of this group give birth to live young, and males frequently exhibit extravagant morphological features and coloration patterns. These characteristics have piqued the interests of biologists that investigate the developmental and evolutionary origins of sex differences as well as a dedicated following of tropical fish hobbyists that appreciate the astonishing diversity within the family.

 

Examples illustrating the diversity of livebearing fish (from the top left to the bottom right): Alfaro cultratus, Brachyrhaphis olomina, Carlhubbsia kidderi, Gambusia eurystoma, Limia perugiae, Phallichthys amates, Mollienesia kykesis, Mollienesia mexicana, Mollienesia sulphuraria, Poeciliposis turrubarensis, Priapella compressa, Priapichthys annectens, Pseudoxiphophorus bimaculatus, Xiphophorus birchmanni, Xiphophorus hellerii, and Xiphophorus variatus


Tackling questions about the effects of sex differences on evolutionary diversification requires the investigation of as many species as possible. The over 250 species of livebearers in the family Poeciliidae are broadly distributed across the Americas, spanning the entire distance from North Carolina in the United States south to Argentina and including the Caribbean Islands. So, although our work has involved field expeditions in various parts of this family’s range, amassing a sufficient amount of species for comparative analyses within a reasonable time period (and with budget limitations) is a nearly impossible task. This study was only possible through the work of generations of fish biologists that have collected specimens and deposited them in museums, where they are accessible for examination by scientists to address questions in environmental biology, ecology, and evolution. In addition, the active community of scientists interested in livebearers have laid a foundation of publically available data on the evolutionary relationships of the family that has facilitated our work.  

The distribution of livebearers (on the left) spans the Americas. To collect data to analyze sex-specific effects on evolutionary diversification, we investigated specimens in museums (top right) and conducted field surveys in different countries (bottom right). 


Leveraging these resources, we have assembled a dataset that includes morphological characteristics for males and females of 112 species, as well as information about male mating strategies, female reproductive strategies, and the ecological niche of each species. We found that morphological diversification in this family did not occur in parallel between the sexes. Instead, pronounced shifts in male and female characteristics occurred in different parts of the phylogenetic tree. In addition, morphological traits consistently evolved faster in males than in females. While female morphology aligned with environmental conditions in their distributional range, male characteristics were primarily related to mating strategies. Thus, discordant patterns and speeds of trait evolution between males and females were primarily driven by females adapting to ambient environmental conditions, and males adapting to different mating strategies. This result indicates that natural and sexual selection have interacted to shape morphological diversification in livebearers. Nonetheless, closely related species have primarily diverged in their ecological niche, but not female reproductive strategies or male mating strategies. This is consistent with adaptation to different environmental conditions being a primary cause for speciation, even though sexual selection played a role in trait evolution. 

From an evolutionary perspective, we have a very good understanding how differences between males and females arise, but we still know little about how sex differences affect broad scale patterns of diversification. Our study highlights that sex differences can profoundly affect the patterns and speed of trait evolution. Considering that sexual dimorphism is pervasive across the animal kingdom, we need to challenge the assumption that the evolution of male and female traits occurs in parallel and explicitly incorporate sex differences – and potential mechanisms that give rise to them – into our analyses.

 

One of our field sites in Mexico harboring multiple species of livebearers that occur in sympatry.

 
The full paper can be found here: http://go.nature.com/2u5koq0

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