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Uncorrected Proofs for Review Only C5478.Indb 28 1/24/11 2:08:33 PM M Chapter 3 Variation and evolution of reproductive strategies Marcelo N. Pires, Amanda Banet, Bart J. A. Pollux, and David N. Reznick 3.1 Introduction sociation between these two traits suggests that one of the two traits might be more likely to evolve when the other he family poeciliidae (Rosen & Bailey 1963) trait is already present (the latter facilitating the evolu- consists of a well-defi ned, monophyletic group of tion of the former). However, the existence of a notable Tnearly 220 species with a fascinating heterogene- exception in the literature (the lecithotrophic, superfetat- ity in life-history traits. Reznick and Miles (1989a) made ing Poeciliopsis monacha, the only known exception at the one of the fi rst systematic attempts to gather information time) showed that superfetation and matrotrophy were not from a widely scattered literature on poeciliid life histo- strictly linked, indicating that these two traits can evolve ries. They focused on two important female reproductive independently of each other. traits: (1) the ability to carry multiple broods at different Reznick and Miles (1989a) also proposed a framework developmental stages (superfetation; Turner 1937, 1940b, for future research that was aimed at evaluating possible 1940c), which tends to cause females to produce fewer off- causes and mechanisms for the evolution of superfetation spring per brood and to produce broods more frequently, and matrotrophy by (1) gathering detailed life-history de- and (2) the provisioning of eggs and developing embryos scriptions of a greater number of poeciliid species, either by the mother, which may occur prior to (lecithotrophy) or through common garden studies or from fi eld-collected after (matrotrophy) fertilization. Their review documented individuals, (2) comparing superfetating species with their the distribution of these two reproductive traits among closest nonsuperfetating relatives (and matrotrophic species poeciliids and their correlates with other life-history traits, with their closest lecithotrophic relatives) to test hypotheses including mean and minimum reproductive size, reproduc- about the ecological conditions under which superfetation tive allocation, brood size, offspring dry weight at birth, (or matrotrophy) should be favored, (3) developing a highly interbrood interval, and mean adult size. resolved, family-wide phylogenetic tree, and (4) applying Their study yielded several new insights. One was that phylogenetic comparative methods (e.g., phylogenetically superfetation may have evolved multiple times within the independent contrasts; Felsenstein 1985) to test for corre- family and appeared to be largely confi ned to the closely lations among different facets of reproductive modes (e.g., allied genera Heterandria, Neoheterandria, and Poeciliop- superfetation, matrotrophy), on the one hand, and to inter- sis. The authors cautioned, however, that their data set was pret either the descriptive life-history traits or the outcome limited by uneven representation of genera. Further knowl- of paired experiments, on the other. edge of other, hitherto-uninvestigated genera was required Over the last 20 years, much action has been taken on before reaching a conclusion that superfetation is confi ned these recommendations. Some of the published work will to these three genera. A second insight was that most spe- be synthesized in this chapter, and occasionally we will cies with superfetation were matrotrophic; the strong as- draw upon our own unpublished data. We concentrate on Uncorrected Proofs for Review Only C5478.indb 28 1/24/11 2:08:33 PM M. N. Pires et al. 29 the evolution of superfetation and postfertilization mater- species, it has been shown that the different size modes cor- nal provisioning (matrotrophy) and address these specifi c respond to genes linked to the Y chromosome that control questions: the age and size at maturity (Kallman 1989). Offspring size (like many other life-history traits) is typi- 1. What are the ranges of variation in some traits that cally related to female body size (Reznick & Miles 1989a); are associated with superfetation and postfertilization some of the smallest offspring are produced by the smallest maternal provisioning (i.e., standard length, offspring species within the family. Most studies express offspring size, brood size, and reproductive allocation) within the size in terms of embryo dry weight, which exhibits a 14- family Poeciliidae (section 3.2)? fold range of variation (mean neonate mass ranging from 2. To what extent do poeciliids vary in their ability to 0.58 mg in Poeciliopsis prolifi ca to 8.3 mg in P. elongata; carry multiple broods (degree of superfetation) and in Pires et al. 2007; Reznick, unpublished data). An increase the amount of postfertilization maternal provisioning in female body size is generally also associated with longer (degree of matrotrophy), and are these traits coupled interbrood intervals in both superfetating and nonsuperfe- (section 3.3)? tating species (Reznick & Miles 1989a). In nonsuperfetat- 3. What are the patterns of life-history variation within ing species, for instance, interbrood interval ranges from the family, and what do they reveal about evolutionary 21.9 days in the small-bodied Poecilia reticulata (Thibault trends of trait evolution in poeciliids (section 3.4)? & Schultz 1978) to 63.8 days in the larger Poecilia lati- 4. What are some of the available hypotheses for the pinna (Hubbs & Dries 2002). In superfetating species, evolution of postfertilization maternal provisioning and there appears to be a similar trend: larger species, such as superfetation, and to what extent are they supported Poeciliopsis gracilis and Poeciliopsis turneri, which on aver- (section 3.5)? age carry two to three broods simultaneously, have an in- terbrood interval of 11–23 days (Thibault & Schultz 1978; Snelson et al. 1986), while the somewhat smaller-bodied 3.2 Life-history variation in the family Poeciliidae Heterandria formosa (Scrimshaw 1944b) and Phallopty- chus januarius (Pollux, unpublished data) can give birth Poeciliids display wide variation in all life-history traits. every 1–3 days to as few as one to fi ve offspring at a time. Here, we briefl y outline the ranges of variation of several Brood size (the number of offspring per brood) is related to life-history traits within the family Poeciliidae known (or female body size in nonsuperfetating species, with larger suspected) to be associated with postfertilization maternal species (as well as larger individuals within species) on provisioning. The genera Cnesterodon, Pamphorichthys, average producing larger broods than their smaller coun- Phalloptychus, and Poecilia (subgenus Acanthophacelus) terparts (e.g., Turner & Snelson 1984; Reznick & Miles contain some of the smallest known species in the family 1989a; Reznick et al. 1992; Reznick et al. 1993). In super- (e.g., mean standard length [SL] for Cnesterodon iguape, fetating species, however, brood size appears to be indepen- male = 19.7 mm, female = 21.4 mm; Pamphorichthys per- dent of female size, both within (e.g., Xenodexia ctenolepis; tapeh, male = 15.9 mm, female = 18.04 mm; Phallopty- Reznick et al. 2007a) and among (Reznick & Miles 1989a) chus januarius, male = 17.3 mm, female = 23.7 mm; Poe- species. In these species, brood size seems to depend more cilia picta, male = 18.3 mm, female = 19.8 mm; Reznick on the degree of superfetation, with highly superfetating et al. 1992; Rosa & Costa 1993; Lucinda 2005b, 2005a; species expected to have smaller broods than similar-sized Figueiredo 2008; Pires et al. 2010). On the other hand, the species that carry fewer simultaneous broods at a time genera Poeciliopsis, Poecilia, and Belonesox have some of (Reznick & Miles 1989a). Taking all poeciliids into ac- the largest poeciliid species (e.g., mean male/female SL of count, there is a remarkable, nearly 100- to 200-fold, 72.4/102.9, 63.8/85.7, 36.0/83.5, and 35.0/66.0 mm for variation in mean brood size, ranging from 1 offspring per Belonesox belizanus, Poecilia catemaconis, Poeciliopsis brood (e.g., H. formosa, Phalloptychus januarius, P. pro- elongata, and Poeciliopsis catemaco, respectively; Miller lifi ca, Gambusia hubbsi; Scrimshaw 1944a; Downhower 1975; Turner & Snelson 1984; Reznick, unpublished data). et al. 2000; Pires et al. 2007; Pollux, unpublished data) to Poeciliids typically show strong size dimorphism, with males over 99 young per brood in B. belizanus (Turner & Snelson being considerably smaller than females (Bisazza 1993a). 1984) and over 200 per brood in Gambusia affi nis (Krum- Despite this size dimorphism, males display a variation in holz 1948). mean SL similar to that of females (approximately fi vefold). Reproductive allocation (RA), defi ned as the percent Mature males within a population often display polymodal of female dry weight that consists of developing embryos, or highly skewed size distributions (Kallman 1989; Kolluru shows a nearly ninefold variation in poeciliids, being as low & Reznick 1996; Arias & Reznick 2000). In some of these as 4.1% in the matrotrophic Phalloceros caudimaculatus Uncorrected Proofs for Review Only C5478.indb 29 1/24/11 2:08:33 PM 30 Chapter 3 (Arias & Reznick 2000) and over 35% in the lecithotro- ing exists and is large enough to be refl ected in some em- phic G. affi nis (Stearns 1983c; Reznick & Braun 1987). bryonic weight gain during development, while the term Finally, it is noteworthy that life-history traits can vary “lecithotrophic” is applied to species in which all
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