Studies Of Mating Systems Research Articles

Female Reproductive Success Variation in a Pseudotsuga menziesii Seed Orchard as Revealed by Pedigree Reconstruction from a Bulk Seed Collection

The impact of female reproductive success on the mating system, gene flow, and genetic diversity of the filial generation was studied using a random sample of 801 bulk seed from a 49-clone Pseudotsuga menziesii seed orchard. We used microsatellite DNA fingerprinting and pedigree reconstruction to assign each seed's maternal and paternal parents and directly estimated clonal reproductive success, selfing rate, and the proportion of seed sired by outside pollen sources. Unlike most family array mating system and gene flow studies conducted on natural and experimental populations, which used an equal number of seeds per maternal genotype and thus generating unbiased inferences only on male reproductive success, the random sample we used was a representative of the entire seed crop; therefore, provided a unique opportunity to draw unbiased inferences on both female and male reproductive success variation. Selfing rate and the number of seed sired by outside pollen sources were found to be a function of female fertility variation. This variation also substantially and negatively affected female effective population size. Additionally, the results provided convincing evidence that the use of clone size as a proxy to fertility is questionable and requires further consideration.

Characterisation of microsatellite markers for the rare and critically endangered Banksia brownii (Proteaceae)

Banksia brownii is a critically endangered small endemic tree restricted to the Stirling Range and Albany area of Western Australia. A genomic library was constructed and novel polymorphic microsatellite markers developed to allow studies of genetic structure, mating systems and gene flow in B. brownii. Markers were assessed in individuals from across the species range and polymorphism further investigated for 12 selected markers in 26 individuals from the Toolbrunup Stirling Range population. Three loci showed significant departure from Hardy–Weinberg equilibrium (P < 0.01) and two of these showed evidence of null alleles. None of the two locus combinations showed evidence of linkage disequilibrium. Levels of polymorphism were moderate in the Toolbrunup population with the number of alleles per locus ranging from two to nine. Observed heterozygosity ranged from 0.200 to 0.957 and expected heterozygosity from 0.308 to 0.849.

Subtle Edge-of-Range Genetic Structuring in Transcontinentally Distributed North American Tree Swallows

Understanding how genetic variation in the Tree Swallow (Tachycineta bicolor) is geographically structured is informative because this broadly distributed North American bird is increasingly used as a model for studies of mating systems, life-history traits, and physiology. We explored patterns of phylogeographic differentiation across the Tree Swallow's breeding range by using nine microsatellite loci and a mitochondrial DNA sequence marker. Contrary to this species' high population-level variation in life-history traits and other ecologically important characteristics, we found no genetic structuring across the majority of its distribution, spanning Tennessee, New York, and Alaska, but we found that birds from California form a distinct yet subtly differentiated genetic cluster. The Tree Swallow can be characterized as a species with both continent-wide genetic panmixia and slight differentiation at one edge of its breeding distribution. This pattern of genetic variation has implications for understanding the underlying basis of geographic variation in this species' life history and other phenotypic traits.

Highly polymorphic microsatellite markers for the short-snouted seahorse (Hippocampus hippocampus), including markers from a closely related species the long-snouted seahorse (Hippocampus guttulatus)

Species of the family Syngnathidae are increasingly being investigated for conservation purposes but also for mating system and genetic parentage studies. The availability of highly polymorphic markers will be of great importance to conduct these kinds of studies. This paper describes the development and characterization of 10 polymorphic microsatellite markers for Hippocampus hippocampus and the utility of nine markers which were developed for a closely related species Hippocampus guttulatus. The number of alleles per locus developed for H. hippocampus ranged from 14 to 30, with levels of heterozygosity between 0.90 and 0.95. Most of the markers were successfully cross-amplified in the sister species, giving clear and unambiguous peaks and maintaining high levels of polymorphism.

Variation in the extra-pair mating systems of Acadian Flycatchers and Wood Thrushes in forest fragments in southern Ontario

The application of molecular tools to studies of avian mating systems has revealed that most songbird species engage in extra-pair matings. However, little is known about the possible effects of habitat fragmentation on extra-pair mating systems. During the breeding seasons of 2002 and 2003, we quantified the frequency of extra-pair matings in Acadian Flycatchers (Empidonax virescens) and Wood Thrushes (Hylocichla mustelina) nesting in forest fragments in southern Ontario. Acadian Flycatchers are at the limit of their northern range in southern Ontario and occurred at low densities (0.005-0.015 males/ha). Across forest fragments, 14% of young Acadian Flycatchers were the result of extra-pair fertilizations. In contrast, Wood Thrushes were common in forest fragments, with breeding densities ranging from 0.37 to 1 males/ha. Extra-pair mating was common among Wood Thrushes, with 40% of young the result of extra-pair matings. Compared to populations studied in less fragmented habitats in Pennsylvania, rates of extra-pair paternity in Ontario were lower for Acadian Flycatchers and higher for Wood Thrushes. Our results demonstrate that rates of extra-pair mating can vary across landscapes. However, the extra-pair mating systems of Acadian Flycatchers and Wood Thrushes appear to respond differently to fragmentation. We suggest that low breeding densities on fragments may be mediating the low rates of extra-pair mating observed in Acadian Flycatchers in southern Ontario, whereas changes to the behavioral tactics of male and female Wood Thrushes in southern Ontario may explain the high levels of extra-pair mating.

Characterization of 35 novel microsatellite loci for ecological and evolutionary studies of the bluntnose minnow (Pimephales notatus)

The bluntnose minnow (Pimephales notatus) is abundant and widespread with a broad ecological niche. This species is also sexually dimorphic with strong competition between males during the mating season. We developed two genomic libraries enriched for microsatellite repeats - one dinucleotide and one tetranucleotide - and isolated 48 putative, novel microsatellite loci. Of those, we present 35 polymorphic and statistically independent microsatellite markers with two to 18 alleles per locus and heterozygosities ranging from 0.04 to 1. These markers will be useful for future behavioural, ecological, evolutionary and mating system studies using P. notatus.

Cross‐species amplification of primers developed from Plantago major and P. intermedia in two Hawaiian Plantago species from the section Plantago

Thirty-nine primers, developed from the sister species Plantago major and P. intermedia, were tested in two Hawaiian Plantago species from the section Plantago. Eight primers were polymorphic, of which three were published earlier, and five are new ones presented here. Amplification and polymorphism levels appeared to be high in these Hawaiian species. These markers will be valuable for further mating system and evolutionary studies in species from the section Plantago that are closely related to P. major and P. intermedia.

Opening Pandora's box: comparative studies of genetic mating systems reveal reproductive complexity

Genetic analyses of realized reproductive success have fundamentally changed our understanding of mating behaviour in natural systems. While behavioural ecologists have long been interested in what factors influence mating behaviour, early studies were limited to direct observations of matings and thus provided an incomplete picture of reproductive activity. Genetic assessments of parentage have revolutionized the study of reproductive behaviour, revealing that many individuals engage in extra-pair copulations (Griffith et al. 2002) and that social mating partners frequently invest substantial resources into raising offspring that are unrelated to one or both of them (Avise et al. 2002). While these findings have changed the way we think about reproductive behaviour, most investigations of genetic parentage have been restricted to single populations at a single point in time, obscuring spatial and/or temporal variation in mating behaviour and limiting our ability to determine how environmental changes can lead to shifts in mating strategies. In this issue of Molecular Ecology, Mobley & Jones (2009) compare genetic mating behaviour across five populations of Syngnathus floridae (Fig. 1), a widespread species of pipefish distributed along the Gulf- and Atlantic Coasts of North America. The authors document how genetic mating behaviour varies across space in S. floridae and identify correlations between reproductive variation and particular ecological characteristics. Mobley & Jones' paper is one of an increasing number of studies which address the question of how ecological variables influence mating behaviour, and highlights how our understanding of mating system variation and evolution is likely to expand through the wider application of high-throughput parentage assessment in a comparative context.

Characterization of 32 novel microsatellite loci for population and mating system studies using Campostoma anomalum (central stoneroller)

The central stoneroller (Campostoma anomalum) is an abundant, widespread and sexually dimorphic stream minnow that is a useful model for mating system studies as well as a sentinel species for understanding population-level processes for fishes in headwater communities. We developed one genomic library enriched for dinucleotide repeats and isolated 48 putative, novel microsatellite loci. Of those, we present 32 polymorphic and independent microsatellite markers with 3 to 16 alleles per locus and heterozygosity ranging from 0.23 to 0.95. Hence, these markers will be useful for future behavioural, ecological and evolutionary studies using C. anomalum.

Bird ringing as a tool for behavioural studies

Birds are an ideal model system for studying many aspects of animal behaviour. Throughout the last 100 years, ringing has been an essential tool in avian behavioural research as it allows birds to be identified and observed on an individual basis. Here, I introduce some of the most important and active research areas, including the study of dispersal, feeding behaviour, mating systems, sociality and vocal communication. This review highlights the pivotal role that ringing will continue to play in developing our knowledge and understanding of animal behaviour and the importance of an organised ringing scheme combining the efforts of volunteer ringers and scientists.

Development of microsatellites from the rare ironstone endemic, Tetratheca paynterae ssp. paynterae and cross‐species amplification

Nineteen microsatellite markers were developed from Tetratheca paynterae ssp. paynterae, a rare and endangered, leafless, perennial shrub. Twelve loci were polymorphic in T. paynterae ssp. paynterae with two to 14 alleles per locus and mean expected heterozygosityof0.62. Primer pairs were tested on four other Tetratheca species from ironstone ranges in southern Western Australia. Ten loci were polymorphic in T. paynterae ssp. cremnobata and T. aphylla ssp. aphylla, three in T. harperi and four in T. erubescens. The level of polymorphism was adequate for studies of genetic structure and mating systems in three of the five taxa.

Twenty‐three microsatellite DNA loci for population genetic studies and parentage assignment in orangethroat darter, Etheostoma spectabile

The genus Etheostoma is a species-rich and ecologically important group of fishes in North America. The orangethroat darter (Etheostoma spectabile) is widely distributed and abundant in headwater streams throughout the central Midwest, and is an excellent model for ecological and mating system studies. We developed 23 novel, polymorphic, and independent microsatellite loci for E. spectabile. We found from two to 14 alleles per locus, and observed heterozygosities ranged from 0.39 to 1.0. These markers, in combination with others isolated from Etheostoma taxa, will be useful for ecological and evolutionary studies in the genus.

Isolation and characterization of polymorphic microsatellite markers in Iberolacerta monticola, and cross‐species amplification in Iberolacerta galani and Zootoca vivipara

Fourteen polymorphic microsatellite loci are described for the Iberian rock lizard, Iberolacerta monticola. Genetic variation in a sample of 20 individuals from Piornedo (northwestern Spain) was quantified both by the number of alleles per locus, which ranged from six to 13, and by the expected frequency of heterozygotes under random mating (heterozygosity), which ranged from 0.761 to 0.902. Single locus and global exclusion probabilities were also computed, and indicate a high power of these markers for paternity assignments and mating system studies of I. monticola. All the analysed loci were also polymorphic in Iberolacerta galani, but only seven in Zootoca vivipara.

Thirty-three microsatellite loci for noninvasive genetic studies of the giant panda (Ailuropoda melanoleuca)

Limited microsatellite markers useable in noninvasive genetic methods have hampered the studies of dispersal patterns and mating systems of giant pandas. Therefore, we describe in this paper the characterization of 15 novel microsatellite loci from genomic DNA-enriched libraries and 18 redesigned microsatellite loci from published papers on the giant panda. The number of alleles per locus in 60 individuals ranged from 2 to 13, the average observed heterozygosity per locus from 0.168 to 0.800, and the average expected heterozygosity per locus from 0.152 to 0.882. All loci followed Hardy-Weinberg expectations. Four pairs of significant linkage association were found among all these loci. Moreover, the 33 microsatellite loci showed high amplification successes rate in noninvasive samples, which indicated that these loci will be of use in studying dispersal patterns and mating systems of giant pandas using noninvasive genetic methods.

A TALE OF TWO CONTINENTS: BAKER'S RULE AND THE MAINTENANCE OF SELF-INCOMPATIBILITY IN LYCIUM (SOLANACEAE)

Over 50 years ago, Baker (1955, 1967) suggested that self-compatible species were more likely than self-incompatible species to establish new populations on oceanic islands. His logic was straightforward and rested on the assumption that colonization was infrequent; thus, mate limitation favored the establishment of self-fertilizing individuals. In support of Baker's rule, many authors have documented high frequencies of self-compatibility on islands, and recent work has solidified the generality of Baker's ideas. The genus Lycium (Solanaceae) has ca. 80 species distributed worldwide, and phylogenetic studies suggest that Lycium originated in South America and dispersed to the Old World a single time. Previous analyses of the S-RNase gene, which controls the stylar component of self-incompatibility, have shown that gametophytically controlled self-incompatibility is ancestral within the genus, making Lycium a good model for investigating Baker's assertions concerning reproductive assurance following oceanic dispersal. Lycium is also useful for investigations of reproductive evolution, given that species vary both in sexual expression and the presence of self-incompatibility. A model for the evolution of gender dimorphism suggests that polyploidy breaks down self-incompatibility, leading to the evolution of gender dimorphism, which arises as an alternative outcrossing mechanism. There is a perfect association of dimorphic gender expression, polyploidy, and self-compatibility (vs. cosexuality, diploidy, and self-incompatibility) among North American Lycium. Although the association between ploidy level and gender expression also holds for African Lycium, to date no studies of mating systems have been initiated in Old World species. Here, using controlled pollinations, we document strong self-incompatibility in two cosexual, diploid species of African Lycium. Further, we sequence the S-RNase gene in 15 individuals from five cosexual, diploid species of African Lycium and recover 24 putative alleles. Genealogical analyses indicate reduced trans-generic diversity of S-RNases in the Old World compared to the New World. We suggest that genetic diversity at this locus was reduced as a result of a founder event, but, despite the bottleneck, self-incompatibility was maintained in the Old World. Maximum-likelihood analyses of codon substitution patterns indicate that positive Darwinian selection has been relatively strong in the Old World, suggesting the rediversification of S-RNases following a bottleneck. The present data thus provide a dramatic exception to Baker's rule, in addition to supporting a key assumption of the Miller and Venable (2000) model, namely that self-incompatibility is associated with diploidy and cosexuality.

PERMANENT GENETIC RESOURCES: Isolation, characterization and multiplex genotyping of 11 autosomal and four sex‐linked microsatellite loci in the reed bunting, Emberiza schoeniclus (Emberizidae, Aves)

Fifteen highly polymorphic microsatellite loci were characterized in the reed bunting, Emberiza schoeniclus. Eleven loci were autosomal and four linked to the Z chromosome. All loci were characterized and tested in 45 unrelated reed buntings from a Swiss population. Autosomal loci displayed seven to 17 and sex-linked loci displayed four to 13 alleles with heterozygosities ranging from 0.756 to 0.933 and from 0.478 to 0.957, respectively. These loci will be used in population genetic and mating system studies of reed buntings.

Modified SLCA Algorithm for Full-Sib Reconstruction of Haplodiploid Species

Full-sib reconstruction from molecular marker data in the absence of parental information is an active research area. Such analyses can provide useful information for studies of mating systems and gene flow, and for estimating effective population size in the wild. Although various methods have been proposed, but their estimation accuracies for some applications are not known. Here we propose a modified version of Shared Loci Correspondence Analysis (mSLCA) to reconstruct full-sib families of haplodiploid species. We ran simulations to compare the accuracies of the original SLCA and mSLCA. mSLCA outperformed SLCA at various data settings. mSLCA produced accurate estimates of the number of full-sib families when the numbers of loci and alleles per locus were equal to or more than eight. We also used actual DNA data of commercial Bombus terrestris colonies to verify the validity of estimates with an increasing number of colonies. mSLCA outperformed SLCA at various colony sizes with slight underestimation.

Microsatellite markers in the endangered Australian northern corroboree frog, Pseudophryne pengilleyi (Anura: Myobatrachidae) and amplification in other Pseudophryne species

Seven microsatellite primer pairs were isolated and characterized in the endangered Australian northern corroboree frog (Pseudophryne pengilleyi). All seven were polymorphic (2–14 alleles) and displayed high heterozygosity (0.036–0.964) in 28 sampled individuals. We also tested the microsatellites on two closely related species. Four were polymorphic in the southern corroboree frog (P. corroboree) and Bibron’s toadlet (P. bibronii). These primers will be useful in studies of conservation genetics and mating systems in Pseudophryne species.

Effect of inbreeding depression on outcrossing rates among populations of a tropical pine

Inbreeding depression is common among plants and may distort mating system estimates. Mating system studies traditionally ignore this effect, nonetheless an assessment of inbreeding depression that may have occurred before progeny evaluation could be necessary. In the neotropical Pinus chiapensis inbreeding depression was evaluated using regression analysis relating progeny F-values with seed germinability, the mating system was analysed in three populations with contrasting size, using isozymes, obtained a corrected outcrossing rate. Selfing decreased seed viability by 19%, relative to an outcrossed plant. Multilocus outcrossing rates, t(m), varied widely among populations. In the two smallest populations t(m) congruent with 1. Therefore, inbreeding depression did not affect the estimates, but overestimated t(m) by 10% in the third population, which has a true mixed mating system (selfing was the major source of inbreeding), and an unusually low t(m) for pines (t(m) = 0.54, uncorrected, t(m) = 0.49, corrected). Inbreeding depression may be an uneven source of bias for outcrossing estimates even at the infraspecific level. Accuracy [corrected] but not precision [corrected] may be gained by including inbreeding depression in outcrossing estimates. Therefore, caution should be taken when comparing t(m) among species or even populations within the same species.

Cross-amplification and characterization of microsatellite loci for three species of Theobroma (Sterculiaceae) from the Brazilian Amazon

This study reports on the cross-species amplification of 23 microsatellite markers previously developed for Theobromacacao L. (Sterculiaceae), source of chocolate in three economically important Amazonian species of Theobroma (T. grandiflorum, T. subincanum, T. sylvestre). Thirteen of the 23 microsatellite loci tested were polymorphic across the three species at 2–13 alleles per locus. The observed heterozygosity per locus varied from 0.18 to 0.84 and expected heterozygosity ranged from 0.28 to 0.87. The high level of transferability and genetic information content of these microsatellite loci indicate their usefulness for population genetic, mating system and breeding studies of these economically important Amazonian fruit trees.