Maternal Investment Influences Expression of Resource Polymorphism in Amphibians: Implications for the Evolution of Novel Resource-Use Phenotypes

Pfennig DW (2010) Maternal Investment Influences Expression of Resource Polymorphism in Amphibians: Implications for the Evolution of Novel Resource-Use Phenotypes. PLoS ONE 5(2): e9117. doi:10.1371/journal.pone.0009117 Maternal Investment Influences Expression of Resource Polymorphism in Amphibians: Implications for the Evolution of Novel Resource-Use Phenotypes Ryan A. Martin 0 David W. Pfennig 0 Stewart Plaistow, University of Liverpool, United Kingdom 0 Department of Biology, University of North Carolina , Chapel Hill, North Carolina , United States of America Maternal effects-where an individual's phenotype is influenced by the phenotype or environment of its mother-are taxonomically and ecologically widespread. Yet, their role in the origin of novel, complex traits remains unclear. Here we investigate the role of maternal effects in influencing the induction of a novel resource-use phenotype. Spadefoot toad tadpoles, Spea multiplicata, often deviate from their normal development and produce a morphologically distinctive carnivore-morph phenotype, which specializes on anostracan fairy shrimp. We evaluated whether maternal investment influences expression of this novel phenotype. We found that larger females invested in larger eggs, which, in turn, produced larger tadpoles. Such larger tadpoles are better able to capture the shrimp that induce carnivores. By influencing the expression of novel resource-use phenotypes, maternal effects may play a largely underappreciated role in the origins of novelty. - A central goal of evolutionary biology is to understand how novel, complex traits arise [1,2]. An organisms external environment often plays a critical role in directing both the development and evolution of novel traits. Specifically, the environment may promote the development of novel traits through phenotypic plasticity (see recent review in [3]), and it may promote the evolution of novel traits through genetic accommodation (sensu [1]). Thus, clarifying how the environment influences the expression and evolution of complex traits is crucial for understanding how new traits arise. Here, we explore the role of the maternal environment in influencing the expression of a novel resource-use phenotype. Understanding how resource-use phenotypes originate is important, because their evolution may permit populations to invade and persist in novel or changing environments [4,5]. Moreover, the evolution of resource polymorphism in which alternative morphs showing differential resource use occur in the same population [4] may represent a critical, early phase in the formation of a new species [1,4,6,7]. We specifically consider how the phenotype of an individuals mother, independent of the effects of her genes, influence which resource-use morph the individual will ultimately express. Little is known about whether and how such maternal effects (sensu [8]) mediate resource polymorphism [4], (but see [9,10] for possible examples). Yet, maternal effects may play a key role in the development and evolution of resource polymorphism, especially in species, such as amphibians, where egg provisioning often constitutes the only maternal investment [11,12], and where a mothers environment can influence the amount (and, possibly, quality) of provision she allocates to each egg [1316]. Such differential investment can, in turn, profoundly affect her offsprings phenotype (reviewed in [12]). For example, larger females often produce larger eggs [1417], which develop into larger, faster developing tadpoles [15,1820]. Furthermore, differential investment may mediate plasticity in the expression of offspring traits [9,19,21,22]. In particular, in species where individuals facultatively express alternative resource-use morphs depending upon their environmental circumstances (e.g., see [2325]), offspring that receive greater maternal investment may induce a different resource-use morph than offspring that receive less maternal investment (e.g., see [9,26]). Thus, maternal effects may often be critical in the expression of resource polymorphism. Previous research by Pfennig and Martin [10] suggests that a condition-dependent maternal effect mediates differences in the expression of resource polymorphism in different populations of an amphibian. In the present study, we examine the proximate mechanisms underlying such a maternal effect. We also speculate on the role maternal effects may play in the evolution of novel resource-use phenotypes. Before outlining our specific objectives, we first describe our study system in more detail. Study System Mexican spadefoot toads (Spea multiplicata: Family Pelobatidae) occur in Mexico and the southwestern U.S. [27]. Their tadpoles are unusual in that they exhibit considerable variation in resource use, morphology, and life history, even within a single clutch. In particular, these tadpoles may develop into either a small, slowly developing tadpole with normal sized jaw muscles used for feeding on detritus at the pond bottom (the omnivore morph), or a larger, more rapidly developing tadpole with greatly enlarged jaw muscles used for feeding on anostracan fairy shrimp in open water (the carnivore morph), [24,2830], (for photos of both morphs, see [31]). The carnivore morph is a novel phenotype within the family Pelobatidae that has arisen only in the genus Spea [5]. Morph determination is environmentally induced. Tadpoles are born as omnivores, but they may develop into carnivores if they ingest anostracan fairy shrimp early in life [24,29,32]. However, there is considerable variation in carnivore production, and some sibships are more prone than others to produce carnivores, even when tadpoles are reared under common conditions [33,34]. Moreover, because shrimp are limited in most natural ponds [30], competition among tadpoles for the more nutritious shrimp prey [35] critically affects the probability that any particular tadpole will eat shrimp and thus experience the cue that induces the carnivore morph [30,36]. This resource polymorphism appears to be maintained evolutionarily as an adaptive response to variation among natural ponds in longevity and resource availability. Carnivores are favored in highly ephemeral ponds where shrimp are most abundant and where a carnivores rapid growth and development increase their likelihood of metamorphosing before their pond dries [24,30]. Omnivores, by contrast, are favored in longer-lasting ponds, where shrimp tend to be scarce [24]. However, both morphs are often present in the same pond [24,28,29]. In such situations, individuals compete for food most with other tadpoles that express the same morphotype [30,37]. As a result, negative frequency-dependent selection favors the rarer morph [30]. Thus, selection to minimize competition for food can maintain both morphs in the same pond. An additional selective agent influencing the evolution of resource polymorphism in this system is interspecific com (...truncated)