Dataset Information

Evolution of microsatellite loci in the adaptive radiation of Hawaiian honeycreepers.

ABSTRACT: Previous studies have examined germ-line mutations to infer the processes that generate and maintain variability in microsatellite loci. Few studies, however, have examined patterns to infer processes that act on microsatellite loci over evolutionary time. Here, we examine changes in 8 dinucleotide loci across the adaptive radiation of Hawaiian honeycreepers. The loci were found to be highly variable across the radiation, and we did not detect ascertainment bias with respect to allelic diversity or allele size ranges. In examining patterns at the sequence level, we found that changes in flanking regions, repeat motifs, or repeat interruptions were often shared between closely related species and may be phylogenetically informative. Genetic distance measures based on microsatellites were strongly correlated with those based on mitochondrial DNA (mtDNA) sequences as well as with divergence time up to 3 My. Phylogenetic inferences based on microsatellite genetic distances consistently recovered 2 of the 4 honeycreeper clades observed in a tree based on mtDNA sequences but differed from the mtDNA tree in the relationships among clades. Our results confirm that microsatellite loci may be conserved over evolutionary time, making them useful in population-level studies of species that diverged from the species in which they were characterized as long as 5 Ma. Despite this, we found that their use in phylogenetic inference was limited to closely related honeycreeper species.

SUBMITTER: Eggert LS

PROVIDER: S-EPMC2734101 | biostudies-literature | 2009 Mar-Apr

REPOSITORIES: biostudies-literature

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Evolution of microsatellite loci in the adaptive radiation of Hawaiian honeycreepers.

Eggert Lori S LS Beadell Jon S JS McClung Andrew A McIntosh Carl E CE Fleischer Robert C RC

The Journal of heredity 20090118 2

Previous studies have examined germ-line mutations to infer the processes that generate and maintain variability in microsatellite loci. Few studies, however, have examined patterns to infer processes that act on microsatellite loci over evolutionary time. Here, we examine changes in 8 dinucleotide loci across the adaptive radiation of Hawaiian honeycreepers. The loci were found to be highly variable across the radiation, and we did not detect ascertainment bias with respect to allelic diversity ...[more]

PMID: 19153085

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Project description:BACKGROUND: The Hawaiian honeycreepers are an avian adaptive radiation containing many endangered and extinct species. They display a dramatic range of phenotypic variation and are a model system for studies of evolution, conservation, disease dynamics and population genetics. Development of a genome-scale resources for this group would augment the quality of research focusing on Hawaiian honeycreepers and facilitate comparative avian genomic research. RESULTS: We assembled the genome sequence of a Hawaii amakihi (Hemignathus virens),and identified ~3.9 million single nucleotide polymorphisms (SNPs) in the genome. Using the amakihi genome as a reference, we also identified ~156,000 SNPs in RAD tag (restriction site associated DNA) sequencing of five honeycreeper species (palila [Loxioides bailleui], Nihoa finch [Telespiza ultima], iiwi [Vestiaria coccinea], apapane [Himatione sanguinea], and amakihi). SNPs are distributed throughout the amakihi genome, and the individual sequenced shows several large regions of low heterozygosity on chromosomes 1, 5, 6, 8 and 11. SNPs from RAD tag sequencing were also found throughout the genome but were found to be more densely located on microchromosomes, apparently a result of differential distribution of the particular site recognized by restriction enzyme BseXI. CONCLUSIONS: The amakihi genome sequence will be useful for comparative avian genomics research and provides a significant resource for studies in such areas as disease ecology, evolution, and conservation genetics. The genome sequences will enable mapping of transcriptome data for honeycreepers and comparison of gene sequences between avian taxa. Researchers will be able to use the large number of SNP markers to genotype honeycreepers in regions of interest or across the whole genome. There are enough markers to enable use of methods such as genome-wide association studies (GWAS) that will allow researchers to make connections between phenotypic diversity of honeycreepers and specific genetic variants. Genome-wide markers will also help resolve phylogenetic and population genetic questions in honeycreepers.

Project description:There is debate about the current population trends and predicted short-term fates of the endangered forest birds, Hawai`i Creeper (Loxops mana) and Hawai`i `?kepa (L. coccineus). Using long-term population size estimates, some studies report forest bird populations as stable or increasing, while other studies report signs of population decline or impending extinction associated with introduced Japanese White-eye (Zosterops japonicus) increase. Reliable predictors of impending population collapse, well before the collapse begins, have been reported in simulations and microcosm experiments. In these studies, statistical indicators of critical slowing down, a phenomenon characterized by longer recovery rates after population size perturbation, are reported to be early warning signals of an impending regime shift observable prior to the tipping point. While the conservation applications of these metrics are commonly discussed, early warning signal detection methods are rarely applied to population size data from natural populations, so their efficacy and utility in species management remain unclear. We evaluated two time series of state-space abundance estimates (1987-2012) from Hakalau Forest National Wildlife Refuge, Hawai`i to test for evidence of early warning signals of impending population collapse for the Hawai`i Creeper and Hawai`i `?kepa. We looked for signals throughout the time series, and prior to 2000, when white-eye abundance began increasing. We found no evidence for either species of increasing variance, autocorrelation, or skewness, which are commonly reported early warning signals. We calculated linear rather than ordinary skewness because the latter is biased, particularly for small sample sizes. Furthermore, we identified break-points in trends over time for both endangered species, indicating shifts in slopes away from strongly increasing trends, but they were only weakly supported by Bayesian change-point analyses (i.e., no step-wise changes in abundance). The break-point and change-point test results, in addition to the early warning signal analyses, support that the two populations do not appear to show signs of critical slowing down or decline.

Project description:We have limited knowledge of the patterns, causes, and prevalence of elevational migration despite observations of seasonal movements of animals along elevational gradients in montane systems worldwide. While a third of extant Hawaiian landbird species are estimated to be elevational migrants this assumption is based primarily on early naturalist's observations with limited empirical evidence. In this study, we compared stable hydrogen isotopes (δ2H) of metabolically inert (feathers) and active (blood plasma, red blood cells) tissues collected from the same individual to determine if present day populations of Hawaiian honeycreepers undergo elevational movements to track areas of seasonally high flower bloom that constitute significant food resources. We also measured stable carbon isotopes (δ13C) and stable nitrogen isotopes (δ15N) to examine potential changes in diet between time periods. We found that the majority of 'apapane (Himatione sanguinea) and Hawai'i 'amakihi (Chlorodrepanis virens) captured at high elevation, high bloom flowering sites in the fall were not year-round residents at the capture locations, but had molted their feathers at lower elevations presumably in the summer after breeding. δ2H values of feathers for all individuals sampled were higher than blood plasma isotope values after accounting for differences in tissue-specific discrimination. We did not find a difference in the propensity of elevational movement between 'apapane and Hawai'i 'amakihi, even though the 'amakihi is considered more sedentary. However, consistent with a more generalist diet, δ15N values indicated that Hawai'i 'amakihi had a more diverse diet across trophic levels than 'apapane, and a greater reliance on nectar in the fall. We demonstrate that collecting multiple tissue samples, which grow at different rates or time periods, from a single individual can provide insights into elevational movements of Hawaiian honeycreepers over an extended time period.

Project description:Background"Explosive" adaptive radiations on islands remain one of the most puzzling evolutionary phenomena. The rate of phenotypic and ecological adaptations is extremely fast during such events, suggesting that many genes may be under fairly strong selection. However, no evidence for adaptation at the level of protein coding genes was found, so it has been suggested that selection may work mainly on regulatory elements. Here we report the first evidence that positive selection does operate at the level of protein coding genes during rapid adaptive radiations. We studied molecular adaptation in Hawaiian endemic plant genus Schiedea (Caryophyllaceae), which includes closely related species with a striking range of morphological and ecological forms, varying from rainforest vines to woody shrubs growing in desert-like conditions on cliffs. Given the remarkable difference in photosynthetic performance between Schiedea species from different habitats, we focused on the "photosynthetic" Rubisco enzyme, the efficiency of which is known to be a limiting step in plant photosynthesis.ResultsWe demonstrate that the chloroplast rbcL gene, encoding the large subunit of Rubisco enzyme, evolved under strong positive selection in Schiedea. Adaptive amino acid changes occurred in functionally important regions of Rubisco that interact with Rubisco activase, a chaperone which promotes and maintains the catalytic activity of Rubisco. Interestingly, positive selection acting on the rbcL might have caused favorable cytotypes to spread across several Schiedea species.SignificanceWe report the first evidence for adaptive changes at the DNA and protein sequence level that may have been associated with the evolution of photosynthetic performance and colonization of new habitats during a recent adaptive radiation in an island plant genus. This illustrates how small changes at the molecular level may change ecological species performance and helps us to understand the molecular bases of extremely fast rate of adaptation during island adaptive radiations.

Project description:The patterns of mutation and evolution at 13 microsatellite loci were studied in the filamentous fungal genus Neurospora. First, a detailed investigation was performed on five microsatellite loci by sequencing each microsatellite, together with its nonrepetitive flanking regions, from a set of 147 individuals from eight species of Neurospora. To elucidate the genealogical relationships among microsatellite alleles, repeat number was mapped onto trees constructed from flanking-sequence data. This approach allowed the potentially convergent microsatellite mutations to be placed in the evolutionary context of the less rapidly evolving flanking regions, revealing the complexities of the mutational processes that have generated the allelic diversity conventionally assessed in population genetic studies. In addition to changes in repeat number, frequent substitution mutations within the microsatellites were detected, as were substitutions and insertion/deletions within the flanking regions. By comparing microsatellite and flanking-sequence divergence, clear evidence of interspecific allele length homoplasy and microsatellite mutational saturation was observed, suggesting that these loci are not appropriate for inferring phylogenetic relationships among species. In contrast, little evidence of intraspecific mutational saturation was observed, confirming the utility of these loci for population-level analyses. Frequency distributions of alleles within species were generally consistent with the stepwise mutational model. By comparing variation within species at the microsatellites and the flanking-sequence, estimated microsatellite mutation rates were approximately 2500 times greater than mutation rates of flanking DNA and were consistent with estimates from yeast and fruit flies. A positive relationship between repeat number and variance in repeat number was significant across three genealogical depths, suggesting that longer microsatellite alleles are more mutable than shorter alleles. To test if the observed patterns of microsatellite variation and mutation could be generalized, an additional eight microsatellite loci were characterized and sequenced from a subset of the same Neurospora individuals.

Dataset Information

Evolution of microsatellite loci in the adaptive radiation of Hawaiian honeycreepers.

Publications

Evolution of microsatellite loci in the adaptive radiation of Hawaiian honeycreepers.

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