The Evolution of Placentas in the Fish Family Poeciliidae: an empirical study of macroevolution

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How and why do new species evolve? How and why do complex organs, like eyes, evolve? These phenomena happen on time scales much longer than our lives, making it difficult for us to understand how they happened. Species are defined by being distinct from and not breeding with each other. Not interbreeding could be a simple matter of when, where or who you choose to mate with. It could also be caused by a failure to produce offspring that can survive and reproduce. Species today are often kept separate from one another by multiple mechanisms, so we do not know how they evolved in the first place. Likewise, complex organs are like machines with many parts that must all be present and well integrated if the machine is to work, but how did this complexity arise? In each case, nature most often presents us with end products without any clues about how they came about; however, sometimes nature provides groups of species that retain enough clues to these processes for one to be able to study how they occur, as in the case of this research program. One impact of this work pertains to the complex organ that is studied. These investigators are studying the evolution of placentas and are doing so in a context in which they can compare species with placentas with close relatives who lack placentas or have less complex placentas. This diversity enables them to address the consequences of having a placenta, including how it affects fertility. The research will enhance the training of students at multiple levels (high school, college, and post-graduate) as well as provide outreach to the public.The proposed research combines work done at two levels of resolution. First, the investigators will work on all species in the fish family Poeciliidae, enabling them to define the timing and order of evolutionary changes. Second, they will perform experiments on individual species within the family to characterize the mechanisms that cause evolution. They will sequence whole genomes then use the DNA sequences to reconstruct the family tree. They will characterize the biology of every species on the tree, including how females provision their young and how males and females choose who to mate with. These fish all bear live young, but some fully provision eggs before they are fertilized while others continue to provision eggs after fertilization. The latter group has the functional equivalent of a mammalian placenta, but species vary in how well the placenta is developed and how much they provision young during development. Species also differ in how they choose mates, with some having males with elaborate ornamentation and courtship displays and others with no sex differences in coloration and no courtship. The integration of biology with the family tree is what will enable the investigators to infer when and in what order female provisioning and aspects of mate choice evolved. It is also possible to test whether the evolution of certain traits is associated with an acceleration or deceleration of how fast new species are formed. It will then be possible to test predictions derived from evolutionary theory for how the evolution of these traits are inter-related with one another. The family tree also enables the investigators to identify closely related species that differ in the presence or absence of placentas. These species pairs become the subjects of experiments in which they will perform more detailed studies of the biology of reproductive isolation, including assessments of multiple mating and the rate of evolution of reproductive isolation. The integration of work done at both levels will enable the investigators to detail how mating systems and mode of reproduction affect the evolution of reproductive isolation, how these different facets of speciation have interacted to shape the evolution of species in the family and how they affect the rate of speciation.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.