Adam G. Jones

Methods of parentage analysis in natural populations

The recent proliferation of hypervariable molecular markers has ushered in a surge of techniques for the analysis of parentage in natural and experimental populations. Consequently, the potential for meaningful studies of paternity and maternity is at an all‐time high. However, the details and implementation of the multifarious techniques often differ in subtle ways that can influence the results of parentage analyses. Now is a good time to reflect on the available techniques and to consider their strengths and weaknesses. Here, we review the leading techniques in parentage analysis, with a particular emphasis on those that have been implemented in readily useable software packages. Our survey leads to some important insights with respect to the utility of the different approaches. This review should serve as a useful guide to anyone who wishes to embark on the study of parentage.

STABILITY OF THE G-MATRIX IN A POPULATION EXPERIENCING PLEIOTROPIC MUTATION, STABILIZING SELECTION, AND GENETIC DRIFT

Abstract. Quantitative genetics theory provides a framework that predicts the effects of selection on a phenotype consisting of a suite of complex traits. However, the ability of existing theory to reconstruct the history of selection or to predict the future trajectory of evolution depends upon the evolutionary dynamics of the genetic variance‐covariance matrix (G‐matrix). Thus, the central focus of the emerging field of comparative quantitative genetics is the evolution of the G‐matrix. Existing analytical theory reveals little about the dynamics of G, because the problem is too complex to be mathematically tractable. As a first step toward a predictive theory of G‐matrix evolution, our goal was to use stochastic computer models to investigate factors that might contribute to the stability of G over evolutionary time. We were concerned with the relatively simple case of two quantitative traits in a population experiencing stabilizing selection, pleiotropic mutation, and random genetic drift. Our results show that G‐matrix stability is enhanced by strong correlational selection and large effective population size. In addition, the nature of mutations at pleiotropic loci can dramatically influence stability of G. In particular, when a mutation at a single locus simultaneously changes the value of the two traits (due to pleiotropy) and these effects are correlated, mutation can generate extreme stability of G. Thus, the central message of our study is that the empirical question regarding G‐matrix stability is not necessarily a general question of whether G is stable across various taxonomic levels. Rather, we should expect the G‐matrix to be extremely stable for some suites of characters and unstable for others over similar spans of evolutionary time.

Microsatellite analysis of maternity and the mating system in the Gulf pipefish Syngnathus scovelli, a species with male pregnancy and sex‐role reversal

Highly variable microsatellite loci were employed to study the mating system of the sexually dimorphic Gulf pipefish Syngnathus scovelli. In this species, like others in the family Syngnathidae, ‘pregnant’ males provide all parental care. Gulf pipefish were collected from one locale in the northern Gulf of Mexico, and internally carried broods of 40 pregnant males were analysed genetically. By comparing multilocus microsatellite fingerprints for the inferred mothers against expected genotypic distributions from the population sample, it was determined that: (i) only one male had received eggs from more than a single female; and (ii) on two separate occasions, two different males had received eggs from the same female. Given the high power to detect multiple matings by males, the first finding indicates that only rarely are individual males impregnated by multiple females during the course of a pregnancy. Conversely, given the lower power to detect multiple matings by females due to sampling constraints, the second finding suggests a high frequency of multiple successful matings by females. Thus, this population of Gulf pipefish displays a polyandrous genetic mating system. The relevance of these genetic findings is discussed with regard to the evolution of secondary sex traits in this species, and in other syngnathids.

Evolution and stability of the G-matrix on a landscape with a moving optimum.

Abstract In quantitative genetics, the genetic architecture of traits, described in terms of variances and covariances, plays a major role in determining the trajectory of evolutionary change. Hence, the genetic variance‐covariance matrix (G‐matrix) is a critical component of modern quantitative genetics theory. Considerable debate has surrounded the issue of G‐matrix constancy because unstable G‐matrices provide major difficulties for evolutionary inference. Empirical studies and analytical theory have not resolved the debate. Here we present the results of stochastic models of G‐matrix evolution in a population responding to an adaptive landscape with an optimum that moves at a constant rate. This study builds on the previous results of stochastic simulations of G‐matrix stability under stabilizing selection arising from a stationary optimum. The addition of a moving optimum leads to several important new insights. First, evolution along genetic lines of least resistance increases stability of the orientation of the G‐matrix relative to stabilizing selection alone. Evolution across genetic lines of least resistance decreases G‐matrix stability. Second, evolution in response to a continuously changing optimum can produce persistent maladaptation for a correlated trait, even if its optimum does not change. Third, the retrospective analysis of selection performs very well when the mean G‐matrix (Ḡ) is known with certainty, indicating that covariance between G and the directional selection gradient (3 is usually small enough in magnitude that it introduces only a small bias in estimates of the net selection gradient. Our results also show, however, that the contemporary Ḡ‐matrix only serves as a rough guide to Ḡ. The most promising approach for the estimation of G is probably through comparative phylogenetic analysis. Overall, our results show that directional selection actually can increase stability of the G‐matrix and that retrospective analysis of selection is inherently feasible. One ?riajor remaining challenge is to gain a sufficient understanding of the G‐matrix to allow the confident estimation of Ḡ.

The Bateman gradient and the cause of sexual selection in a sex–role–reversed pipefish

As a conspicuous evolutionary mechanism, sexual selection has received much attention from theorists and empiricists. Although the importance of the mating system to sexual selection has long been appreciated, the precise relationship remains obscure. In a classic experimental study based on parentage assessment using visible genetic markers, more than 50 years ago A. J. Bateman proposed that the cause of sexual selection in Drosophila is ‘the stronger correlation, in males (relative to females), between number of mates and fertility (number of progeny)’. Half a century later, molecular genetic techniques for assigning parentage now permit mirror–image experimental tests of the ‘Bateman gradient’ using sex–role–reversed species. Here we show that, in the male–pregnant pipefish Syngnathus typhle, females exhibit a stronger positive association between number of mates and fertility than do males and that this relationship responds in the predicted fashion to changes in the adult sex ratio. These findings give empirical support to the idea that the relationship between mating success and number of progeny, as characterized by the Bateman gradient, is a central feature of the genetic mating system affecting the strength and direction of sexual selection.

The genetic mating system of a sex-role-reversed pipefish (Syngnathus typhle): a molecular inquiry

Abstract In the pipefish Syngnathus typhle as in other species of Syngnathidae, developing embryos are reared on the males ventral surface. Although much laboratory research has been directed toward understanding sexual selection in this sex-role-reversed species, few studies have addressed the mating behavior of S. typhle in the wild, and none has capitalized upon the power of molecular genetic assays. Here we present the first direct assessment of the genetic mating system of S. typhle in nature. Novel microsatellite loci were cloned and characterized from this species, and employed to assay entire broods from 30 pregnant, field-captured males. Genetic analysis of 1340 embryos revealed that 1–6 females (meanu2009=u20093.1) contributed to each brooded clutch, the highest rate of multiple maternity yet documented in any pipefish. Evidence of multiple mating by females was also detected. Thus, this population of S. typhle displays a polygynandrous mating system, a finding consistent with previous field and laboratory observations. Our results, considered together with similar studies of other syngnathid species, provide preliminary support for the hypothesis that the genetic mating system is related to the evolution of sexual dimorphism in the fish family Syngnathidae.

Validation of Bateman's principles: a genetic study of sexual selection and mating patterns in the rough-skinned newt

Few studies have influenced thought on the nature of sexual selection to the extent of the classic paper of A. J. Bateman on mating patterns in Drosophila. However, interpretation of his study remains controversial, and a lack of modern empirical evidence prevents a consensus with respect to the perceived utility of Batemans principles in the study of sexual selection. Here, we use a genetic study of natural mating patterns in the rough–skinned newt, Taricha granulosa, to investigate the concordance between Batemans principles and the intensity of sexual selection. We found that males experienced strong sexual selection on tail height and body size, while sexual selection was undetectable in females. This direct quantification of sexual selection agreed perfectly with inferences that are based on Batemans principles. Specifically, males (in comparison with females) exhibited greater standardized variances in reproductive and mating success, as well as a stronger relationship between mating success and reproductive success. Overall, our results illustrate that Batemans principles provide the only quantitative measures of the mating system with explicit connections to formal selection theory and should be the central focus of studies of mating patterns in natural populations.

Microsatellite evidence for monogamy and sex‐biased recombination in the Western Australian seahorse Hippocampus angustus

Four polymorphic microsatellite loci were used to assess biological parentage of 453 offspring from 15 pregnant males from a natural population of the Western Australian seahorse Hippocampus angustus. Microsatellite genotypes in the progeny arrays were consistent with a monogamous mating system in which both females and males had a single mate during a male brooding period. Multilocus genotypes implicated four females in the adult population sample as contributors of eggs to the broods of collected males, but there was no evidence for multiple mating by females. Based on genotypic data from the progeny arrays, two loci were linked tightly and the recombination rate appeared to be ≈ 10‐fold higher in females than in males. The utility of linked loci for parentage analyses is discussed.

A microsatellite assessment of sneaked fertilizations and egg thievery in the fifteenspine stickleback

Attempts by males to steal fertilizations from other males are common in many species. In some sticklebacks, males also are known to steal eggs from the nests of rivals and to carry them back to their own nests. However the genetic consequences of these nest‐raiding behaviors seldom have been investigated. Here we assess genetically the prevalence of sneaked fertilizations and egg stealing, and we describe the mating system in a natural population of the fifteenspine stickleback. Six microsatellite markers were developed and employed to assay a total of 1307 embryos from 28 nests. Guardian males and all nest‐holding males in the local area also were genotyped for two to six loci Analysis of male genotypes and those of embryos revealed that five of the 28 nests (18%) contained progeny from sneaked fertilizations, and that four of the 24 nests (17%) with resident males contained stolen egg clutches Comparisons of the composite DNA genotypes of nest‐holding males against those of inferred sneakers implicated one nest holder as the sneaker of a nest seven meters from his own. Also, the genetic data demonstrated that nests of males frequently contain eggs from multiple females. The multilocus genotypes of inferred mothers indicated that females mate with multiple males, sometimes over distances greater than one kilometer.

Sexually selected females in the monogamous Western Australian seahorse

Studies of sexual selection in monogamous species have hitherto focused on sexual selection among males. Here, we provide empirical documentation that sexual selection can also act strongly on females in a natural population with a monogamous mating system. In our field-based genetic study of the monogamous Western Australian seahorse, Hippocampus subelongatus, sexual selection differentials and gradients show that females are under stronger sexual selection than males: mated females are larger than unmated ones, whereas mated and unmated males do not differ in size. In addition, the opportunity for sexual selection (variance in mating success divided by its mean squared) for females is almost three times that for males. These results, which seem to be generated by a combination of a male preference for larger females and a female-biased adult sex ratio, indicate that substantial sexual selection on females is a potentially important but under-appreciated evolutionary phenomenon in monogamous species.