The following research program was initiated in 1988.   It was initially supported by personal funds and small grants from the Academic Senate of the University of California.  It was then supported by:
                        2004-2009   National Science Foundation (DEB-0416085).  The evolution of
placentas in the Poeciliid Fishes: An empirical study of the evolution of complexity.  PI-
David Reznick.  Co-PIs – Mark Springer, Theodore Garland.  $800,000 plus $36,000 in
REU supplements

            I am currently seeking new support to expand on this research program.  I submitted a pre-proposal to the National Science Foundation in January 2014 and was invited to submit a full proposal, due 4 August 2014. The themes of the new research will build on our paper currently in press in Nature that addresses predictions derived from Zeh and Zeh’s viviparity driven conflict hypothesis.  Those predictions pertain to how the conflicts associated with placental reproduction can shape the balance between pre- and post-copulatory reproductive isolation. 
            A byproduct of this research program is that I and my students have become interested in the more general phenomenon of intergenomic conflict. 

Background and Description:
            One of the prominent unanswered questions in evolutionary biology is “what defines the relationship between microevolution and macroevolution”?   Microevolution is the sort of evolution that is modeled with theoretical population genetics and is quantified in nature as a change in allele frequency over time.  Macroevolution represents the longer term, larger scale changes that we associated with evolution, like the origin of new species or the origin of complex organs.  The question is whether natural selection alone can account for both scales of change or if some other process must be invoked to explain macroevolution. 
            The empirical study of macroevolution is generally constrained by the time scale over which macroevolution happens, since it happens on a time frame that is much greater than our own life spans.  A consequence of studying traits with ancient origins is that what we have available for study in living organisms does not give us appropriate material to work with.  For example, there is great interest in the mammalian placenta and how it evolved, but all living placental mammals are derived from a single common ancestor that lived over 100 million years ago. That mammal does not represent the origin of the placenta.  The placenta evolved somewhere along the earlier 100 million year history that separates placental mammals from the marsupials.  This means that we can study the way mammalian placentas work and how they have varied in living mammals, but living mammals cannot give us any information about how and why the placenta evolved. Those events have been lost to history.  The same is true of virtually all complex organs.  Fish in the family Poeciliidae give us the opportunity to perform an empirical study of macroevolution.
            As a byproduct of my work on guppies, I became interested in the life histories of all of the fishes in the family Poeciliidae.  All but one species in this family bear live young. Prior to my work, it had also been found that some of them have the equivalent of a mammalian placenta.  I and my colleagues have now generated descriptions of the mode of maternal provisioning in over 150 species of Poeciliidae.  Rob Meredith and Mark Springer have also generated a DNA-based phylogenetic tree for the family. The tree includes representatives from throughout the order Cyprinodontiformes, additional species outside of this order, and several calibration points derived from the fossil record.  We have combined this tree with the life history data to show that there have been at least eight independent origins of placentas in the family. We can also identify clades of closely related species that contain species with and without placentas.  We are currently reconstructing the pattern of evolution of life histories throughout the order (which includes to additional origins of livebearing and at least two additional origins of matrotrophy). We are also addressing key hypotheses associated with the evolution of placentation. One of those hypotheses is that the evolution of the placenta will in turn cause an accelerated evolution of reproductive isolation and speciation.
            I and my students have also performed a series of experiments to address hypotheses posed by others for the evolution of the placenta.  We have concentrated on clades that include closely related placental and non-placental species so that we can make multiple paired comparisons between the two forms of maternal provisioning.  Making multiple comparisons means that we can also arrive at more general conclusions concerning the biological causes and consequences of the evolution of placentas.
            One key result, represented by one published paper(Pires, Bassar et al. 2011) and one paper in preparation (Bassar et al., 2014, in press) addressed a family of hypotheses that we grouped under the umbrella of “life history facilitation hypotheses”, or hypotheses that the placenta evolved to facilitate the evolution of some other feature of the life history, such as offspring size or age at maturity. These two papers together falsify the generality of any such hypothesis.
            A second set of papers addressed an assumption that was a key part of Trexler and DeAngelis’ model for the evolution of matrotrophy (Trexler and DeAngelis 2003).  Their assumption was that females that have the equivalent of a placenta are also able to strategically abort or retain embryos in response to resource availability. The bigger picture is that an advantage of placentation might be that little in the way of resources is required to initiate an brood of offspring. Most maternal investment follows the fertilization of the egg.  If mothers can regulate how many babies they bring through development in response to resource availability, then the conditions that favor the evolution of matrotrophy are relatively easy to satisfy. If they cannot, then the conditions are much more difficult to fulfill.  In a series of papers (Reznick, Callahan et al. 1996; Banet, Au et al. 2009; Banet, Au et al. 2010; Pollux and Reznick 2011) we showed that females in four different species that represent four independent origins of placentas cannot abort embryos in response to food restrictions experienced during the development of those embryos.  These results severely restrict the circumstances that might favor the evolution of a placenta.
            A byproduct of this work is that we can now define some rules of placentation, at least for placentation in these fishes.  Placental mothers are tethered to developing offspring.  If they experience food restrictions while offspring are developing, then will necessarily give birth to smaller offspring. If food availability instead increases, offspring size will increase.  Pollux and Reznick (2011) show this rule in a very dramatic way with a two-way manipulation of resource availability in Phalloptychus januarius, a placental species from Brazil.  A consequence of these rules is that placental species appear to respond to fluctuating food availability in an inappropriate fashion. Work on a diversity of organisms shows that larger offspring are superior to smaller offspring if they are born into an environment where food availability is low.  Guppies, which are non-placental, are able to adjust offspring size in response to maternal food availability, such that they will produce larger offspring when food availability is low(Reznick and Yang 1993; Reznick, Callahan et al. 1996).  Bashey has now shown that what had been seen in other organisms is also true of guppies, which is that these larger offspring have higher fitness in a competitive environment, where food is scarce, but have no fitness advantage when food is abundant(Bashey 2002; Bashey 2006; Bashey 2008).  If the same rules apply to these placental species, then these rules of placentation mean that they will produce smaller, less fit offspring when food is scarce.
            Overall, our work to date has failed to reveal any adaptive value to placentation.  This does not mean that the placenta may not be adaptive in some as yet unanticipated way, but it does cause us to take more seriously the suggestion that the placenta evolves as a consequence of intergenomic conflict (Crespi and Semeniuk 2004).  Our current research will address such conflict hypotheses.
            Our most recent research (Pollux et al., Nature, in press as of 5/2014) exploits our now having a well-resolved phylogeny for the family Poeciliidae.   We have integrated data in maternal provisioning, sexual dichromatism, male ornamentation, courtship behavior, gonapodium length and sexual size dimorphism to evaluate the patterns of association between the presence of placentation and the development of traits associated with pre-copulatory mate choice.  Zeh and Zeh (Zeh and Zeh 2000; Zeh and Zeh 2008) predicted that the evolution of viviparity and post-fertilization maternal provisioning will be associated with a shift from pre- to post-copulatory mate choice.  Our results show that placentation is indeed associated with a significant reduction in traits associated with mate choice by females.  Our proposed research is designed to further test predictions derived from their conceptual model.
           

Literature Cited

Banet, A. I., A. G. Au, et al. (2009). "Testing an assumption of a model for the evolution of placentas." Integrative and Comparative Biology 49: E9-E9.
Banet, A. I., A. G. Au, et al. (2010). "Is mom in charge?  Implications of resource provisioning on the evolution of the placenta." Evolution 64(11): 3172-3182.
Bashey, F. (2002). Causes and consequences of offspring size variation in the Trinidadian guppy (Poecilia reticulata). Biology. Riverside, California, University of California: 196.
Bashey, F. (2006). "Cross-generational environmental effects and the evolution of offspring size in the Trinidadian guppy Poecilia reticulata." Evolution 60(2): 348-361.
Bashey, F. (2008). "Competition as a selective mechanism for larger offspring size in guppies." Oikos 117(1): 104-113.
Crespi, B. and C. Semeniuk (2004). "Parent-offspring conflict in the evolution of vertebrate reproductive mode." American Naturalist 163(5): 635-653.
Pires, M. N., R. D. Bassar, et al. (2011). "Why do placentas evolve? An evaluation of the life-history facilitation hypothesis in the fish genus Poeciliopsis." Functional Ecology 25(4): 757-768.
Pollux, B. J. A. and D. N. Reznick (2011). "Matrotrophy limits a female's ability to adaptively adjust offspring size and fecundity in fluctuating environments." Functional Ecology 25(4): 747-756.
Reznick, D. N., H. Callahan, et al. (1996). "Maternal effects on offspring quality in poeciliid fishes." American Zoologist 36: 147-156.
Reznick, D. N. and A. P. Yang (1993). "The influence of fluctuating resources on life history: patterns of allocation and plasticity in female guppies." Ecology 74: 2011-2019.
Trexler, J. C. and D. L. DeAngelis (2003). "Resource allocation in offspring provisioning: An evaluation of the conditions favoring the evolution of matrotrophy." American Naturalist 162(5): 574-585.
Zeh, D. W. and J. A. Zeh (2000). "Reproductive mode and speciation: the viviparity-driven conflict hypothesis." Bioessays 22(10): 938-946.
Zeh, J. A. and D. W. Zeh (2008). Viviparity-driven Conflict More to Speciation than Meets the Fly. Year in Evolutionary Biology 2008: 126-148.