Malcolm D. Schug

The distribution and frequency of microsatellite loci in Drosophila melanogaster

We report the results of a comprehensive search of Drosophila melanogaster DNA sequences in GenBank for di‐, tri‐, and tetranucleotide repeats of more than four repeat units, and a DNA library screen for dinucleotide repeats. Dinucleotide repeats are more abundant (66%) than tri‐ (30%) or tetranucleotide (4%) repeats. We estimate that 1917 dinucleotide repeats with 10 or more repeat units are present in the euchromatic D. melanogaster genome and, on average, they occur once every 60 kb. Relative to many other animals, dinucleotide repeats in D. melanogaster are short. Tri‐ and tetranucleotide repeats have even fewer repeat units on average than dinucleotide repeats. Our WorldWide Web site (http://www.bio.cornell.edu/genetics/aquadro/aquadro.html) posts the complete list of 1298 microsatellites (≥ five repeat units) identified from the GenBank search. We also summarize assay conditions for 70 D. melanogaster microsatellites characterized in previous studies and an additional 56 newly characterized markers.

Condition-dependent control of paternity by female purple martins: implications for coloniality

Abstract Proposed causal links between extra-pair copulation (EPC) and colony formation in socially monogamous birds hinge on the question of which sex controls fertilizations. We examined in colonial purple martins Progne subis (1) whether EPCs were forced or accepted by females, and (2) the degree to which apparently receptive females were able to obtain EPCs against their mates’ paternity defenses. Paternity analyses of multilocus DNA fingerprinting confirmed previous findings of a marked relationship between age class and extra-pair fertilizations (EPFs), with young males losing paternity of 43% (n = 53) of their putative offspring compared to 4% (n = 85) by old males. All assignable extra-pair offspring were sired by old males, with one male obtaining most EPFs each year. Contrary to the hypothesis that EPCs are forced, EPF frequency within age class did not increase with seasonal increases in the number of males per fertile female. Whereas the male control hypothesis predicted that the male age class that mate-guarded more would be cuckolded less, the reverse was true: young males guarded significantly more intensely. The male age class difference in cuckoldry could not be explained by the possibility that young and inexperienced females (which are usually paired to young males) were more vulnerable to forced copulation because EPFs were unrelated to female age. These findings suggest that females (1) pair with old males and avoid EPCs, or (2) pursue a mixed mating strategy of pairing with young males and accepting EPCs from old males. The receptivity to EPCs by females paired to young males put them in conflict with their mates. Two factors determined the paternity achieved by young males: (1) the relative size of the male to the female, with young males achieving much higher paternity when they were larger than their mates, and (2) the intensity of mate-guarding. Both variables together explained 77% of the variance in paternity and are each aspects of male-female conflict. Given female receptivity to EPCs, mate-guarding can be viewed as male interference with female mating strategies. We conclude that EPCs are rarely or never forced, but the opportunity for females paired to young males to obtain EPCs is relative to the ability of their mates to prevent them from encountering other males. Evidence of mixed mating strategies by females, combined with other features of the martin mating system, is consistent with the female-driven “hidden lek hypothesis” of colony formation which predicts that males are drawn to colonies when females seek extra-pair copulations.

Microsatellite variation in populations of Drosophila pseudoobscura and Drosophila persimilis.

We have isolated, characterized and mapped 33 dinucleotide, three trinucleotide and one tetranucleotide repeat loci from the four major chromosomes of Drosophila pseudoobscura. Average inferred repeat unit length of the dinucleotide repeats is 12 repeat units, similar to D. melanogaster. Assays of D. pseudoobscura and populations of its sibling species, D. persimilis, using 10 of these loci show extremely high levels of variation compared with similar studies of dinucleotide repeat variation in D. melanogaster populations. The high levels of variation are consistent with an average mutation rate of approximately 10(-6) per locus per generation and an effective population size of D. pseudoobscura approximately four times larger than that of D. melanogaster. Consistent with allozymes and nucleotide sequence polymorphism, the dinucleotide repeat loci reveal minimal structure across four populations of D. pseudoobscura. Finally, our preliminary recombinational mapping of 24 of these microsatellites suggests that the total recombinational genome size may be larger than previously inferred using morphological mutant markers.

MUTATION AND EVOLUTION OF MICROSATELLITES IN DROSOPHILA MELANOGASTER

Levels of nucleotide polymorphism in the Drosophila melanogaster genome are correlated with rates of recombination. This relationship may be due to hitchhiking of advantageous mutations (selective sweeps) or to continual removal of deleterious mutations from the genome (background selection). One test of the relative contributions of selective sweeps and background selection to the observed levels of variation in the genome of D. melanogaster is to compare levels of nucleotide variability (with a mutation rate on the order of 10-9 per nucleotide per generation) with more rapidly evolving DNA loci such as microsatellites. This test depends critically on details of the mutational process of microsatellites. In this paper, we summarize our studies of microsatellite characteristics and mutation rates in D. melanogaster. We find that D. melanogaster microsatellites are short and have a mutation rate (6.5 × 10-6 per locus per generation) several orders of magnitude lower than mammals studied to date. We further show that genetic variation at 18 dinucleotide repeat microsatellites in a population of D. melanogaster from Maryland is correlated with regional rates of recombination. These and other microsatellite data suggest that both background selection and selective sweeps may contribute to the correlation between DNA sequence variation and recombination in Drosophila.

The Genetic Structure of Drosophila ananassae Populations From Asia, Australia and Samoa

Information about genetic structure and historical demography of natural populations is central to understanding how natural selection changes genomes. Drosophila ananassae is a widespread species occurring in geographically isolated or partially isolated populations and provides a unique opportunity to investigate population structure and molecular variation. We assayed microsatellite repeat-length variation among 13 populations of D. ananassae to assess the level of structure among the populations and to make inferences about their ancestry and historic biogeography. High levels of genetic structure are apparent among all populations, particularly in Australasia and the South Pacific, and patterns are consistent with the hypothesis that the ancestral populations are from Southeast Asia. Analysis of population structure and use of F-statistics and Bayesian analysis suggest that the range expansion of the species into the Pacific is complex, with multiple colonization events evident in some populations represented by lineages that show no evidence of recent admixture. The demographic patterns show isolation by distance among populations and population expansion within all populations. A morphologically distinct sister species, D. pallidosa, collected in Malololelei, Samoa, appears to be more closely related to some of the D. ananassae populations than many of the D. ananassae populations are to one another. The patterns of genotypic diversity suggest that many of the individuals that we sampled may be morphologically indistinguishable nascent species.

Studying paternity and paternal care: the value of negative results

Copyright 1998 The Association for the Study of Animal Behaviour

Do blood parasites affect paternity, provisioning and mate-guarding in Purple Martins ?

We examined hypothetical relationships between blood parasite infection in Purple Martins Progne subis and extra-pair paternity of males, feeding performance of parents of both sexes, and mate-guarding intensity of males. We found no evidence that infection with either of two parasites, Haemoproteus prognei and an unspecified microfilariad, affected extra-pair paternity. Infected males were no more likely than uninfected males to be cuckolded, and infection did not preclude extrapair fertilization success. Infection also was unrelated to provisioning rates by adult males and females and to mate-guarding intensity by males. However, subadult females provisioned significantly less when infected with Haemoproteus, suggesting that young females have a lower resistance to parasites than adult females, or males.