Why do placentas evolve? An evaluation of thelife-history facilitation hypothesis in the fish genusPoeciliopsisMarcelo N. Pires*, Ronald D. Bassar, Kevin E. McBride, John U. Regus, Theodore Garland, Jrand David N. ReznickDepartment of Biology, University of California, Riverside, California, 900 University Avenue, Riverside, CA 92521, USASummary1. The Northern Clade of the fish genus Poeciliopsis includes six closely related species, three ofwhich lack placentas and three that have placentas but vary in the extent of post-fertilizationprovisioning.2. We used this diversity to evaluate a series of hypotheses proposed in earlier publications con-cerning why the placenta has evolved. All hypotheses share the attribute of arguing that the pla-centa evolved to enhance the evolution of some other life-history trait, such as to reduce the ageat maturation or to increase offspring size. We refer to these hypotheses collectively as ‘life-his-tory facilitation hypotheses’.3. A general way to evaluate the plausibility of such proposals is to ask whether the evolution ofthe placenta is predictably associated with the evolution of other components of the life history.4. We evaluated such associations in two ways. First, we performed a multivariate analysis oflife-history data for fish collected and preserved in nature. This analysis included 16 populationsacross all six species. Sec ondly, we performed a more complete quantification of the life historiesof the laboratory descendents from five populations representing four species, then performed asimilar multivariate analysis. The laboratory study added information about the timing of repro-duction (age at maturity, frequency of reproduction).5. Both analyses yielded similar results, which were that the evolution of increased placentationis correlated with the evolution of a smaller size at first reproduction, the production of fewerand smaller offspring per litter, but an increase in the number of litters that were developingsimultaneously in the ovary (superfetation). Increased placentation is associated with progres-sively earlier ages at maturation and shorter intervals between the birth of successive litters ofoffspring. Overall, increased placentation was associated with an increase in the rate of produc-tion of offspring early in life. A peculiar attribute of placentation is that this increase in the rateof offspring production can be attained despite a simultaneous reducti on in the proportionalquantity of resources devoted to reproduction.6. These trends support one of the life history facilitation hypotheses, which is that placentationfacilitates earlier maturity and a higher rate of reproduction early in life. They also suggest a pos-sible connection be tween the evolution of the placenta and the well-established theory of life-his-tory evolution, since these same life history attributes are predicted to evolve in response toexposure to high extrinsic rates of adult mortality.Key-words: adaptation, life-history evolution, maternal effect, phenotypic plasticity, preda-tion, reproductive strategies, placenta, placentationIntroductionThe ability of mothers to provide nourishment to develop-ing embryos by a source other than yolk (matrotrophy) isnot an exclusive trait of the mammalia; it is widespreadacross animal taxa (e.g. terrestrial and aquatic gastropods,Baur 1994; Von Rintelen & Glaubrecht 2005; clams, Kor-niushin & Glaubrecht 2003; pseudoscorpions, Makioka1968; flies, Meier, Kotrba & Ferrar 1999; cockroaches,Williford, Stay & Bhattacharya 2004; isopods, Warburg &*Correspondence author. E-mail: [email protected] 2011 The Authors. Functional Ecology  2011 British Ecological SocietyFunctional Ecology 2011, 25, 757–768 doi: 10.1111/j.1365-2435.2011.01842.xRosenberg 1996; several fish groups, Wourms, Grove &Lombardi 1988; amphibians, Greven 1998; Wake 1993;among others). Organisms exhibiting this resource alloca-tion strategy are believed to be subject to unique biologicalconsequences when compared with organisms that areviviparous but only allocate resources in the form of yolk tofeed developing young (lecithotrophy). For example, theevolution of matrotrophic reproduction is expected to alterthe dynamics of life-history trade-offs (Trexler & DeAngelis2003) and costs and benefits of parental care (Smith &Wootton 1995; Reynolds, Goodwin & Freckleton 2002).Placental reproduction is a specialized form of matrotro-phy. The placenta is defined as an apposition of maternal andembryonic tissue that provides for the nourishment of thedeveloping embryo and sustains its metabolic needs (respira-tion and excretion) throughout development (Mossman1937). Placental matrotrophy is hypothesized to intensifymaternal effects because of the prolonged and intimate con-tact between the mother and developing young (Trexler 1985;Korsgaard & Weber 1989; Lombardi 1996; Paulesu, Ro-magnoli & Bigliardi 2005). Moreover, the evolution of pla-cental reproduction may open a new arena for parent–offspring conflict (Haig 1993; Crespi & Semeniuk 2004).Besides mammals, placental organisms include scorpions(Farley 1998), onychophorans (Huebner & Lococo 1994),bivalves (Korniushin & Glaubrecht 2003), bryozoans (Woo-llacott & Zimmer 1975), squamate reptiles (Flemming &Blackburn 2003), and chondrichthyan and osteichthyanfishes (Wourms, Grove & Lombardi 1988; Reynolds, Good-win & Freckleton 2002).Studies of life-history evolution address how traits like theage at maturity, reproductive effort or offspring size mayevolve in response to features of the environment, but havedone little to explore matrotrophic reproduction as a life-his-tory trait, as evidenced by the absence of any discussion ofthis aspect of the life history in the most recent comprehensivereviews (Roff 1992, 2002; Stearns 1992). Trexler & DeAngelis(2003) simulated the fitness costs and benefits of matrotrophyand found that matrotrophy is more likely to evolve in envi-ronments where food availability is constantly high – a pre-diction that is consistent with some earlier proposals(Thibault & Schultz 1978) and empirical results (Reznick,Callahan & Llauredo 1996; Trexler 1997; Swain & Jones2000; Marsh-Matthews & Deaton 2006; Pires, McBride &Reznick 2007).Some authors have proposed a possible bridge between theevolution of matrotrophy and the evolution of other life-his-tory attributes by suggesting that the evolution of matrotro-phy enhances the evolution of other