The evolution of the placenta drives a shift in sexual selection in livebearing fish.

The evolution of the placenta from a non-placental ancestor causes a shift of maternal investment from pre- to post-fertilization, creating a venue for parent-offspring conflicts during pregnancy. Theory predicts that the rise of these conflicts should drive a shift from a reliance on pre-copulatory female mate choice to polyandry in conjunction with post-zygotic mechanisms of sexual selection. This hypothesis has not yet been empirically tested. Here we apply comparative methods to test a key prediction of this hypothesis, which is that the evolution of placentation is associated with reduced pre-copulatory female mate choice. We exploit a unique quality of the livebearing fish family Poeciliidae: placentas have repeatedly evolved or been lost, creating diversity among closely related lineages in the presence or absence of placentation. We show that post-zygotic maternal provisioning by means of a placenta is associated with the absence of bright coloration, courtship behaviour and exaggerated ornamental display traits in males. Furthermore, we found that males of placental species have smaller bodies and longer genitalia, which facilitate sneak or coercive mating and, hence, circumvents female choice. Moreover, we demonstrate that post-zygotic maternal provisioning correlates with superfetation, a female reproductive adaptation that may result in polyandry through the formation of temporally overlapping, mixed-paternity litters. Our results suggest that the emergence of prenatal conflict during the evolution of the placenta correlates with a suite of phenotypic and behavioural male traits that is associated with a reduced reliance on pre-copulatory female mate choice.

Heterochrony in the evolution of Trinidadian guppy offspring size: maturation along a uniform ontogenetic trajectory.

The size and maturity of Trinidadian guppy (Poecilia reticulata) offspring vary among populations adapted to environments of differential predation. Guppy offspring born to low-predation, high-competition environments are larger and more mature than their high-predation ancestors. Here we ask: what specific changes in developmental or birth timing occur to produce the larger, more mature neonates? We collected specimens across the perinatal window of development from five populations and quantified musculoskeletal maturation. We found that all populations undergo similar ontogenetic trajectories in skeletal and muscle acquisition; the only difference among populations is when neonates emerge along the trajectory. The smallest neonates are born with 20% of their skeleton ossified, whereas the largest neonates are born with over 70% of their skeleton ossified. The area of the major jaw-closing muscle is relatively larger in larger offspring, scaling with length as L2.5 The size range over which offspring are birthed among populations sits along the steepest part of the size-maturity relationship, which provides a large marginal increase in fitness for the high-competition female. Because of the functional effects of producing more mature offspring at birth, offspring size may be the first and most critical life-history trait selected upon in highly competitive environments.

Comparative life histories of fishes in the subgenus Limia (Pisces: Poeciliidae).

This study presents life-history descriptions for 12 species in the subgenus Limia, which are endemic to the Greater Antilles. All species in this study lack evidence of superfoetation, producing a single brood of offspring before developing subsequent broods. Interbrood intervals (number of days between parturition events) are also consistent with intervals of species that lack superfoetation. Maternal provisioning, characterized by matrotrophy index, is <1.0 for all species of Limia. This is consistent with species that provide little or no maternal provisioning to developing embryos after ovum fertilization (lecithotrophic). Four species exhibit potentially bi-modal size distributions of mature males. Work on other poeciliids suggests that such bimodal distributions can be caused by genetic polymorphisms in some species. Principle component analyses revealed an axis of interspecific variation in life histories that separated species with small size at maturity and the production of many, small offspring from those with large size at maturity and that produce few, large offspring. This pattern of life-history diversity occurs in many other groups of organisms.

Comparative life histories of fishes in the genus Phallichthys (Pisces: Poeciliidae).

This study presents a description of the life histories of all four species of the genus Phallichthys, found primarily in the Atlantic slope of Central America (ranging from northern Panama to Mexico), based on a combination of data collected from preserved and living specimens. All species produced a single litter of offspring before developing another brood (i.e. no superfoetation). In the laboratory, the mean time interval between successive litters ranged from 24 to 48 days, further suggesting that they lack superfoetation. Embryos lose from 15 to 65% of their dry mass during development, meaning all or the large majority of resources required for development are provided prior to fertilization (lecithotrophy). All mature male size distributions were platykurtotic and appeared either bimodal or multimodal. Multimodal and skewed size distributions have been associated with genetic polymorphisms for size at maturity in other species of Poeciliidae. As the sister clade to Phallichthys includes genera in which all species have superfoetation (Neoheterandria and Poeciliopsis), these results suggest that their common ancestor with Phallichthys also had superfoetation and that the trait has been lost.

The genetic and environmental basis of adaptive differences in shoaling behaviour among populations of Trinidadian guppies, Poecilia reticulata.

The degree of plasticity an individual expresses when moving into a new environment is likely to influence the probability of colonization and potential for subsequent evolution. Yet few empirical examples exist where the ancestral and derived conditions suggest a role for plasticity in adaptive genetic divergence of populations. Here we explore the genetic and plastic components of shoaling behaviour in two pairs of populations of Poecilia reticulata (Trinidadian guppies). We contrast shoaling behaviour of guppies derived from high- and low-predation populations from two separate drainages by measuring the shoaling response of second generation laboratory-reared individuals in the presence and absence of predator induced alarm pheromones. We find persistent differences in mean shoaling cohesion that suggest a genetic basis; when measured under the same conditions high-predation guppies form more cohesive shoals than low-predation guppies. Both high and low-predation guppies also exhibit plasticity in the response to alarm pheromones, by forming tighter, more cohesive shoals. These patterns suggest a conserved capacity for adaptive behavioural plasticity when moving between variable predation communities that are consistent with models of genetic accommodation.

Life-history evolution in guppies. VII. The comparative ecology of high- and low-predation environments.

Prior research has demonstrated a strong association between the species of predators that co-occur with guppies and the evolution of guppy life histories. The evolution of these differences in life histories has been attributed to the higher mortality rates experienced by guppies in high-predation environments. Here, we evaluate whether there might be indirect effects of predation on the evolution of life-history patterns and whether there are environmental differences that are correlated with predation. To do so, we quantified features of the physical and chemical environment and the population biology of guppies from seven high- and low-predation localities. We found that high-predation environments tend to be larger streams with higher light levels and higher primary productivity, which should enhance food availability for guppies. We also found that guppy populations from high-predation environments have many more small individuals and fewer large individuals than those from low-predation environments, which is caused by their higher birth rates and death rates. Because of these differences in size distribution, guppies from high-predation environments have only one-fourth of the biomass per unit area, which should also enhance food availability for guppies in these localities. Guppies from high-predation sites allocate more resources to reproduction, grow faster, and attain larger asymptotic sizes, all of which are consistent with higher levels of resource availability. We conclude that guppies from high-predation environments experience higher levels of resource availability in part because of correlated differences in the environment (light levels, primary productivity) and in part as an indirect consequence of predation (death rates and biomass density). These differences in resource availability can, in turn, augment the effect of predator-induced mortality as factors that shape the evolution of guppy life-history patterns. We found no differences in the invertebrate communities from high- and low-predation localities, so we conclude that there do not appear to be multitrophic, indirect effects associated with these differences in predation.

Life history evolution in guppies (Poecilia reticulata): guppies as a model for studying the evolutionary biology of aging.

Natural populations of guppies can be found with different communities of predators. We have contrasted the early life history of guppies from high and low predation localities. Life history theory predicts that such differences in mortality pattern will select for evolutionary changes in the guppy's life history. Specifically, guppies in high-predation localities are predicted to mature at an earlier age and devote more of their resources to reproduction. We have demonstrated the predicted differences in life history patterns with experiments and observations on guppies from each type of locality. We have also selected for the predicted changes in the life history by manipulating mortality patterns in natural populations. Theories for the evolution of senescence predict that these same mortality patterns will also select for changes in the rate of aging. Specifically, guppies from high-predation localities should have higher rates of aging than their counterparts from low-predation localities. Experiments that select for changes in the early life history should also select for changes in the rate of aging. The existing work on guppies, therefore, presents the opportunity to use them as a new experimental system for studying the evolutionary biology of aging. Finally, I present preliminary results from a pilot study of aging in guppies. This study differs from the earlier work by Comfort because these fish have been reproductively active since they attained maturity; Comfort's fish were maintained as virgins throughout their lives. This study makes two important points. First, age-specific changes in reproductive performance represent as important an index of aging as mortality rates. Second, the rate of aging may be far more rapid in reproductively active individuals.

The evolution of senescence in natural populations of guppies (Poecilia reticulata): a comparative approach.

Model organisms like Drosophila melanogaster or Caenorhabditis elegans have revealed genes that influence senescence and the evolvability of senescence. We are interested instead in evaluating why and how senescence evolves in natural populations. To do so, we are taking the ecological geneticist's perspective of comparing natural populations that differ in factors that are predicted to influence the evolution of senescence and are evaluating whether senescence has evolved in the predicted fashion. We are also manipulating the environment to evaluate more directly the evolution of senescence. Guppies (Poecilia reticulata) are found in streams throughout the Northern Range mountains of Trinidad. Natural populations experience large differences in mortality rate as a consequence of the predators with which they co-occur. We have already shown, both with comparative studies and manipulations of the distribution of guppies and their predators, that the early life history evolves very rapidly in response to these differences in mortality. For example, high adult mortality rates select for individuals that develop more rapidly, produce their first litter of young at an earlier age, and devote more of their available resources to reproduction for the remainder of their lives. These changes were predicted by independently derived theory. Aspects of this same theory also predict how the late life history and senescence should evolve. Specifically, theory predicts that the populations that experience low mortality rates should also experience delayed senescence and longer life spans relative to those that experience high mortality rates. We are currently evaluating these predictions with representatives from two high-predation and two low-predation environments. Our presentation will focus on our pilot study, which evaluated life span, lifetime reproduction, and the patterns of aging in our laboratory populations. We will also report on the progress in our ongoing comparative studies of senescence in natural populations.

Fat cycling in the mosquitofish (Gambusia affinis): fat storage as a reproductive adaptation.

We argue, based on reviewed literature covering reptiles, amphibians, birds, and fish, that fat storage may represent a life history adaptation because it enables an organism to shift in time when resources are allocated to reproduction. We applied these arguments to fat and population cycles in three populations of the mosquito fish, Gambusia affinis. For males, there appeared to be a constant size at maturation during the reproductive season. Mature males became scarce late in the summer. At the same time, immature males delayed maturity and attained much larger sizes; they matured in large numbers in the fall. The amount of stored fat tended to be equal for immature and mature males at all times except in the late summer. In the August samples, when mature males were relatively rare, they also had the lowest level of fat reserves. It appears that the older generation of mature males did not store fat and did not overwinter. At the same time, immature males registered a two to three fold increase in fat reserves. These differences in fat content between mature and immature males disappeared by September, probably because of the recruitment of a new generation of mature males. The reserves were gradually utilized during the winter. Females reproduced from the late spring through mid- to late-summer. They stopped reproducing in the late summer, when there was ample time to produce an additional litter of young. There was an inverse relationship between resources devoted to reproduction and fat reserves. As reproductive allotment decreased in the late summer, fat reserves increased. The magnitude of the change in fat reserves was similar to that displayed by males. The reserves were depleted over the winter. Significant reserves remained at the beginning of the reproductive season the following spring. Reproducing females utilized the remaining reserves significantly more rapidly than non-reproducing females. An analysis of resource availability revealed an overall decrease in food availability in the late summer, coincident with the increase in fat reserves. These cycles are therefore not attributable to changes in resource availability. They instead indicate a change in how resources are allocated by the fish. The trends in the data indicate that fat reserves are used to shift investment in reproduction from the late summer to the following spring. In males, deferring maturity, rather than maturing in August, allows them to store the necessary reserves to survive the winter so that they can mate the following spring. In females, a subset of the fat reserves is intended for producing the first clutch of eggs the following spring. The female pattern corresponds to those reported for a diversity of organisms. The possible advantages of shifting reproductive effort from the fall to the following spring include higher fecundity and higher offspring fitness. The limitations of the methodology and potential directions for future research are discussed.

Parallel evolution of the sexes? Effects of predation and habitat features on the size and shape of wild guppies.

Environmental gradients often lead to the parallel evolution of populations and species. To what extent do such gradients also lead to parallel evolution of the sexes? We used guppies (Poecilia reticulata) to examine the parallel and independent (sex-specific) aspects of population divergence in response to predation and habitat features. Geometric morphometrics was used to analyse size and shape variation for 1335 guppies from 27 to 31 sites sampled in each of 2 years. Body size showed strong parallel population divergence; both sexes were larger at sites with a more open canopy and with higher flow. Body shape showed a mixture of parallel and independent population divergence. The strongest and most consistent effects were (1) high-predation sites had males with smaller heads and deeper caudal peduncles, (2) open-canopy sites had females with smaller heads and more distended abdomens and (3) high-flow sites had males and females with smaller heads and deeper caudal peduncles.

Genetic and environmental effects on secondary sex traits in guppies (Poecilia reticulata).

Male guppies (Poecilia reticulata) exhibit extreme phenotypic and genetic variability for several traits that are important to male fitness, and several lines of evidence suggest that resource level affects phenotypic expression of these traits in nature. We tested the hypothesis that genetic variation for male secondary sex traits could be maintained by genotype-specific effects of variable resource levels (genotype-environment interaction). To do this, we measured genetic variation and covariation under two environmental conditions--relatively low and relatively high food availability. We found high levels of genetic variation for most traits, but we only found a significant G x E interaction across food levels for one trait (body size) for one population. The across-environment correlations for size were large and positive, indicating that the reaction norms for size did not cross. We also found that male colour pattern elements had nearly an order of magnitude more genetic variation than did male size. Heritability estimates indicated that Y-linked genes are responsible for some of the genetic variation in male size and colour traits. We discuss implications of these results for theories of the maintenance of genetic variation in male secondary sexual traits in guppies.

New model systems for studying the evolutionary biology of aging: crustacea.

Progress in any area of biology has generally required work on a variety of organisms. This is true because particular species often have characteristics that make them especially useful for addressing specific questions. Recent progress in studying the evolutionary biology of senescence has been made through the use of new species, such as Caenorhabditis elegans and Drosophila melanogaster, because of the ease of working with them in the laboratory and because investigators have used theories for the evolution of aging as a basis for discovering the underlying mechanisms. I describe ways of finding new model systems for studying the evolutionary mechanisms of aging by combining the predictions of theory with existing information about the natural history of organisms that are well-suited to laboratory studies. Properties that make organisms favorable for laboratory studies include having a short generation time, high fecundity, small body size, and being easily cultured in a laboratory environment. It is also desirable to begin with natural populations that differ in their rate of aging. I present three scenarios and four groups of organisms which fulfill these requirements. The first two scenarios apply to well-documented differences in age/size specific predation among populations of guppies and microcrustacea. The third is differences among populations of fairy shrimp (Anostraca) in habitat permanence. In all cases, there is an environmental factor that is likely to select for changes in the life history, including aging, plus a target organism which is well-suited for laboratory studies of aging.

The population ecology of contemporary adaptations: what empirical studies reveal about the conditions that promote adaptive evolution.

Under what conditions might organisms be capable of rapid adaptive evolution? We reviewed published studies documenting contemporary adaptations in natural populations and looked for general patterns in the population ecological causes. We found that studies of contemporary adaptation fall into two general settings: (1) colonization of new environments that established newly adapted populations, and (2) local adaptations within the context of a heterogeneous environments and metapopulation structure. Local ecological processes associated with colonizations and introductions included exposure to: (1) a novel host or food resource; (2) a new biophysical environment; (3) a new predator community; and (4) a new coexisting competitor. The new environments that were colonized often had depauperate communities, sometimes because of anthropogenic disturbance. Local adaptation in heterogeneous environments was also often associated with recent anthropogenic changes, such as insecticide and herbicide resistance, or industrial melanism. A common feature of many examples is the combination of directional selection with at least a short-term opportunity for population growth. We suggest that such opportunities for population growth may be a key factor that promotes rapid evolution, since directional selection might otherwise be expected to cause population decline and create the potential for local extinction, which is an ever-present alternative to local adaptation. We also address the large discrepancy between the rate of evolution observed in contemporary studies and the apparent rate of evolution seen in the fossil record.

Big houses, big cars, superfleas and the costs of reproduction.

The assumption of costs of reproduction were a logical necessity for much of the early development of life history theory. An unfortunate property of 'logical necessities' is that it is easy to also assume that they must be true. What if this does not turn out to be the case? The existence and universality of costs of reproduction were initially challenged with empirical data of questionable value, but later with increasingly strong theoretical and empirical results. Here, we discuss Ken Spitze's 'superfleas', which represent what we consider to be the strongest empirical challenge to the universality of costs, then offer a possible explanation for their existence.

Identification of major histocompatibility complex genes in the guppy, Poecilia reticulata.

The guppy, Poecilia reticulata, a teleostean fish of the order Cyprinodontiformes, has been used extensively in studies of host-parasite interactions, courtship behavior, and mating preference, as well as in ecological and evolutionary genetics. A related species was among the first poikilotherm vertebrates to be used in the study of histocompatibility genes. All these studies could benefit from the identification and characterization of the guppy major histocompatibility complex (Mhc) genes. Here, both class I and class II genes of the guppy are described. The number of expressed loci, as determined by representation of clones in a cDNA library, sequencing, and Southern blot analysis, may be low in both Mhc classes: combined evidence suggests that there may be one expressed class II locus only and one or two expressed class I loci. The variability of aquaristic guppy stocks is very low: only three and two genes have been detected at the class I and class II loci, respectively, in the stocks examined. This genetic paucity is most likely the consequence of breeding practices employed by aquarists and commercial establishments. Limited sampling of wild guppy populations revealed extensive Mhc polymorphism at loci of both classes in nature. Comparison of guppy Mhc sequences with those of other vertebrates has revealed the existence of a set of insertions/deletions which can be used as characters in cladistic analysis to infer phylogenetic relationships among vertebrate taxa and the Mhc genes themselves. These indels are particularly frequent in the regions coding for the loops of alpha 1 and alpha 2 domains of class I proteins.