Showing papers by "John C. Avise published in 2001"
TL;DR: This volume focuses on genetic studies of the mating systems and reproductive patterns of turtles, specifically with respect to multiple paternity and long-term sperm storage.
Abstract: As evidenced by the articles in this volume, a recent increase in interest in the mating systems of poikilothermic vertebrates has focused primarily on fishes, a few amphibians, and squamate reptiles. Turtles by contrast have received relatively little attention, yet they display a wide variety of mating behaviors and life-history characteristics that make them excellent candidates for addressing several aspects of genetic parentage that should contribute to a broader understanding of animal reproductive strategies. Here we focus on genetic studies of the mating systems and reproductive patterns of turtles, specifically with respect to multiple paternity and long-term sperm storage. These phenomena highlight the importance of a temporally extended perspective on patterns of individual reproductive success.
212 citations
TL;DR: A simple mathematical model is developed showing that sneaking in this polygynous sand goby population almost certainly decreases the opportunity for sexual selection, an outcome that contrasts with the usual effects of cuckoldry in socially monogamous animals.
Abstract: Alternative mating strategies are common in nature and are generally thought to increase the intensity of sexual selection. However, cuckoldry can theoretically decrease the opportunity for sexual selection, particularly in highly polygamous species. We address here the influence of sneaking (fertilization thievery) on the opportunity for sexual selection in the sand goby Pomatoschistus minutus, a marine fish species in which males build and defend nests. Our microsatellite-based analysis of the mating system in a natural sand goby population shows high rates of sneaking and multiple mating by males. Sneaker males had fertilized eggs in ≈50% of the assayed nests, and multiple sneakers sometimes fertilized eggs from a single female. Successful males had received eggs from 2 to 6 females per nest (mean = 3.4). We developed a simple mathematical model showing that sneaking in this polygynous sand goby population almost certainly decreases the opportunity for sexual selection, an outcome that contrasts with the usual effects of cuckoldry in socially monogamous animals. These results highlight a more complex and interesting relationship between cuckoldry rates and the intensity of sexual selection than previously assumed in much of the literature on animal mating systems.
159 citations
TL;DR: Genetic studies of the genetic mating systems of pipefishes and seahorses have provided insights into important aspects of the natural history and evolution of these fishes, and suggest that the sexual selection gradient (or Bateman gradient) may be a substantially better method for characterizing the mating system than previously available techniques.
Abstract: In pipefishes and seahorses (family Syngnathidae), the males provide all postzygotic care of offspring by brooding embryos on their ventral surfaces. In some species, this phenomenon of male "pregnancy" results in a reversal of the usual direction of sexual selection, such that females compete more than males for access to mates, and secondary sexual characteristics evolve in females. Thus the syngnathids can provide critical tests of theories related to the evolution of sex differences and sexual selection. Microsatellite-based studies of the genetic mating systems of several species of pipefishes and seahorses have provided insights into important aspects of the natural history and evolution of these fishes. First, males of species with completely enclosed pouches have complete confidence of paternity, as might be predicted from parental investment theory for species in which males invest so heavily in offspring. Second, a wide range of genetic mating systems have been documented in nature, including genetic monogamy in a seahorse, polygynandry in two species of pipefish, and polyandry in a third pipefish species. The genetic mating systems appear to be causally related to the intensity of sexual selection, with secondary sex characters evolving most often in females of the more polyandrous species. Third, genetic studies of captive-breeding pipefish suggest that the sexual selection gradient (or Bateman gradient) may be a substantially better method for characterizing the mating system than previously available techniques. Finally, these genetic studies of syngnathid mating systems have led to some general insights into the occurrence of clustered mutations at microsatellite loci, the utility of linked loci in studies of parentage, and the use of parentage data for direct estimation of adult population size.
138 citations
TL;DR: Overall, genetic markers have both confirmed and quantified the incidence of several reproductive and other social behaviors of fishes, and have thereby enhanced the knowledge of piscine natural history.
Abstract: Molecular analyses of bird and mammal populations have shown that social mating systems must be distinguished from genetic mating systems. This distinction is important in fishes also, where the potential for extrapair spawning and intraspecific brood parasitism is especially great. We review studies on fishes that have used molecular markers to document biological parentage and genetic mating systems in nature, particularly in species with extended parental care of offspring. On average, nest-guarding adults parented about 70-95% of their custodial offspring, and approximately one-third of the nests were cuckolded to some extent. Furthermore, nearly 10% of the assayed nests contained offspring tended by foster fathers either because of nest takeovers or egg thievery. On average, fish that provide parental care on nests spawned with more mates than did fish with internal fertilization and pregnancy. Overall, genetic markers have both confirmed and quantified the incidence of several reproductive and other social behaviors of fishes, and have thereby enhanced our knowledge of piscine natural history.
114 citations
TL;DR: Microsatellite markers are employed to assess genetic paternity in successive clutches of individually marked, free-ranging female painted turtles over a four year period and suggest a ‘last in, first out’ operation of the females’ sperm storage tubules.
Abstract: Most studies of genetic parentage in natural populations have been limited to a single breeding season or reproductive episode and, thus, provide only a snapshot of individuals' mating behaviours. Female turtles can store viable sperm in their reproductive tracts for as long as several years, but the extent to which this capacity is utilized in nature has remained unknown. Here, we employ microsatellite markers to assess genetic paternity in successive clutches of individually marked, free-ranging female painted turtles (Chrysemys picta) over a four year period. The genetic data from 113 clutches from this natural population demonstrate that most females (80.5%) remated each year and that each female generally used a single male's sperm to fertilize all clutches laid within a year. However, sperm usage among females varied considerably, and some females apparently used sperm that had been stored for up to three years to fertilize some or all eggs laid in consecutive nesting seasons. Thus, remating by females is not necessary for continued offspring production from a given sire. Furthermore, 13.2% of all clutches examined showed evidence of multiple paternity, and the genetic paternity patterns across years suggest a 'last in, first out' operation of the females' sperm storage tubules.
104 citations
TL;DR: To help visualize functional operations in such intracellular genomic societies and to better encapsulate the evolutionary origins of complex genomes, new and evocative metaphors may be both entertaining and research-stimulating.
Abstract: Recent genome-sequencing efforts have confirmed that traditional "good-citizen" genes (those that encode functional RNA and protein molecules of obvious benefit to the organism) constitute only a small fraction of the genomic populace in humans and other multicellular creatures. The rest of the DNA sequence includes an astonishing collection of noncoding regions, regulatory modules, deadbeat pseudogenes, legions of repetitive elements, and hosts of oft-shifty, self-interested nomads, renegades, and immigrants. To help visualize functional operations in such intracellular genomic societies and to better encapsulate the evolutionary origins of complex genomes, new and evocative metaphors may be both entertaining and research-stimulating.
86 citations
TL;DR: A DNA–based study of parentage in the Gulf pipefish Syngnathus scovelli is used to show that sexual selection indeed acts more strongly on females than on males in this species, and exhibits classical polyandry with the greatest asymmetry in reproductive roles yet documented in any system.
Abstract: Due to the phenomenon of male pregnancy, the fish family Syngnathidae (seahorses and pipefishes) has historically been considered an archetypal example of a group in which sexual selection should act more strongly on females than on males. However, more recent work has called into question the idea that all species with male pregnancy are sex-role reversed with respect to the intensity of sexual selection. Furthermore, no studies have formally quantified the opportunity for sexual selection in any natural breeding assemblage of pipefishes or seahorses in order to demonstrate conclusively that sexual selection acts most strongly on females. Here, we use a DNA-based study of parentage in the Gulf pipefish Syngnathus scovelli in order to show that sexual selection indeed acts more strongly on females than on males in this species. Moreover, the Gulf pipefish exhibits classical polyandry with the greatest asymmetry in reproductive roles (as quantified by variances in mating success) between males and females yet documented in any system. Thus, the intensity of sexual selection on females in pipefish rivals that of any other taxon yet studied.
84 citations
TL;DR: The ecological setting appears not to be predictive of alternative male mating strategies, a finding of relevance to sexual selection theory.
Abstract: Molecular markers have proved extremely useful in resolving mating patterns within individual populations of a number of species, but little is known about how genetic mating systems might vary geographically within a species. Here we use microsatellite markers to compare patterns of sneaked fertilization and mating success in two populations of sand goby (Pomatoschistus minutus) that differ dramatically with respect to nest-site density and the documented nature and intensity of sexual selection. At the Tvarminne site in the Baltic Sea, the microsatellite genotypes of 17 nest-tending males and mean samples of more than 50 progeny per nest indicated that approximately 35% of the nests contained eggs that had been fertilized by sneaker males. Successful nest holders mated with an average of 3.0 females, and the distribution of mate numbers for these males did not differ significantly from the Poisson expectation. These genetically deduced mating-system parameters in the Tvarminne population are remarkably similar to those in sand gobies at a distant site adjoining the North Sea. Thus, pronounced differences in the ecological setting and sexual selection regimes in these two populations have not translated into evident differences in cuckoldry rates or other monitored patterns of male mating success. In this case, the ecological setting appears not to be predictive of alternative male mating strategies, a finding of relevance to sexual selection theory.
77 citations
TL;DR: Results demonstrate that such genetic data on parentage can be helpful not only in estimating contemporary population sizes, but also in providing additional information, not present in customary mark–recapture data, about possible extended movements of breeding individuals and the size of the pool of mates which they encounter.
Abstract: Molecular polymorphisms have been used in a variety of ways to estimate both effective and local census population sizes in nature. A related approach for estimating the current size of a breeding population, explored here for the first time, is the use of genetic 'marks' reconstructed for otherwise unknown parents in paternity or maternity analyses of progeny arrays. This method provides interesting similarities and contrasts to traditional mark-recapture methods based on physical tags. To illustrate, this genetic method is applied to a population of painted turtles on the Mississippi River to estimate the number of successfully breeding males. Non-genetic mark-recapture approaches were also applied to animals trapped at this location. Results demonstrate that such genetic data on parentage can be helpful not only in estimating contemporary population sizes, but also in providing additional information, not present in customary mark-recapture data, about possible extended movements of breeding individuals and the size of the pool of mates which they encounter.
65 citations
TL;DR: The genetic results suggest that the evolutionary elaboration of the enclosed brood pouch elsewhere in the family was probably not in response to selection pressures on pregnant males to avoid fertilization thievery, and the polyandrous genetic mating system in this species parallels the social mating system.
Abstract: Highly variable microsatellite loci were used to study the mating system of Nerophis ophidion, a species of pipefish in which pregnant males carry embryos on the outside of their body rather than in an enclosed brood pouch. Despite this mode of external fertilization and brooding, otherwise rare in the family Syngnathidae, the genotypes of all embryos proved to be consistent with paternity by the tending male, thus indicating that cuckoldry by sneaker males is rare or nonexistent in this species. N. ophidion is a phylogenetic outlier within the Syngnathidae and its reproductive morphology is thought to be close to the presumed ancestral condition for pipefishes and seahorses. Thus, our genetic results suggest that the evolutionary elaboration of the enclosed brood pouch elsewhere in the family was probably not in response to selection pressures on pregnant males to avoid fertilization thievery. With regard to maternity assignments, our genotypic data are consistent with behavioural observations indicating that females sometimes mate with more than one male during a breeding episode, and that each male carries eggs from a single female. Thus, the polyandrous genetic mating system in this species parallels the social mating system, and both are consistent with a more intense sexual selection operating on females, and the elaboration of secondary sexual characters in that gender.
53 citations
TL;DR: The authors' molecular results clearly indicate that guardian males do indeed consume their own genetic offspring, even when unrelated (foster) embryos are present within the nest, and suggest that the phenomenon may result, at least in part, from an inability of guardians to differentiate between kin and nonkin within their own nests.
Abstract: Cannibalism is widespread in natural populations of fishes, where the stomachs of adults frequently contain conspecific juveniles. Furthermore, field observations suggest that guardian males routinely eat offspring from their own nests. However, recent genetic paternity analyses have shown that fish nests often contain embryos not sired by the nest-tending male (because of cuckoldry events, egg thievery, or nest piracy). Such findings, coupled with the fact that several fish species have known capabilities for distinguishing kin from nonkin, raise the possibility that cannibalism by guardian males is directed primarily or exclusively toward unrelated embryos in their nests. Here, we test this hypothesis by collecting freshly cannibalized embryos from the stomachs of several nest-tending darter and sunfish males in nature and determining their genetic parentage by using polymorphic microsatellite markers. Our molecular results clearly indicate that guardian males do indeed consume their own genetic offspring, even when unrelated (foster) embryos are present within the nest. These data provide genetic documentation of filial cannibalism in nature. Furthermore, they suggest that the phenomenon may result, at least in part, from an inability of guardians to differentiate between kin and nonkin within their own nests.
TL;DR: Computer programs designed to count the number of gametotypes contributed by unshared parents to each such progeny array, as well as assess the accuracy and precision of various estimators for the true number of un shared parents via computer simulation, are introduced.
Abstract: Molecular technologies have made feasible large-scale studies of genetic parentage in nature by permitting the genotypic examination of hundreds or thousands of progeny. One common goal of such studies is to estimate the true number of unshared parents who contributed to a large half-sib progeny array. Here we introduce computer programs designed to count the number of gametotypes contributed by unshared parents to each such progeny array, as well as assess the accuracy and precision of various estimators for the true number of unshared parents via computer simulation. These simulations indicate that under most biological conditions (1) a traditional approach (the multilocus MINIMUM METHOD) that merely counts the number of distinct haplotypes in offspring and divides by 2L, where L is the number of loci assayed, often vastly underestimates the true number of unshared parents who contributed to a half-sib progeny array; (2) a recently developed HAPLOTYPES estimator is a considerable improvement over the MINIMUM METHOD when parental numbers are high; and (3) the accuracy and precision of the HAPLOTYPES estimator increase as marker polymorphism and sample size increase, or as reproductive skew and the number of parents contributing to the progeny array decrease. Generally, HAPLOTYPES-based estimates of parental numbers in large half-sib cohorts should improve the characterization of organismal reproductive strategies and mating systems from genetic data.