Severe Bottleneck Research Articles

Spatial genetics of wild tomato species reveals roles of the Andean geography on demographic history

Understanding the demographic history of natural populations in relation to the geographic features in their habitats is an important step toward deciphering the mechanisms of evolutionary processes in nature. This study investigates how the complex geographic and ecological features of the Andes play a role in demographic history, species divergence, dispersal patterns, and hybridization in wild tomato species. We investigated spatial genetics of two closely related wild tomato species, Solanum lycopersicum and S. pimpinellifolium, by integrating amplified fragment length polymorphism (AFLP) marker data and geographic information system (GIS)-derived geographic and climatic data. The two species represent genetically distinct lineages largely separated by the Andes, but hybridize extensively in central to northern Ecuador, likely mediated by the transitional climatic conditions between those of the two species. Solanum lycospericum has likely experienced a severe population bottleneck during the colonization of the eastern Andes followed by a rapid population expansion. The study demonstrates that the evolutionary patterns of the two wild tomatoes, including demographic history, dispersal patterns, interspecific divergence, and hybridization, are intimately related to the complex geographic and ecological features of the Andes. Integrating genetic data across the genome and GIS-derived environmental data can provide insights into the patterns of complex evolutionary processes in nature.

231 SEMINAL QUALITY IN WHOOPING CRANE (GRUS AMERICANA) IS AFFECTED BY STAGE OF BREEDING SEASON BUT NOT BY AGE OF INDIVIDUAL

The whooping crane is one of the most critically endangered species in North America. The species underwent a severe genetic bottleneck with only 16 individuals remaining in the wild as of 1942. Captive breeding began in 1966 and continues to produce chicks for release in order to establish new wild populations. However, captive birds experience poor reproduction with approximately 40% of eggs being infertile. Males have been known to reach sexual maturity at 5 years of age and continue to reproduce almost as long as the duration of their adult life (i.e. 40 years). Understanding factors affecting seminal quality may assist in identifying and correcting causes of suboptimal reproduction. Our objectives were to determine the influence of age and reproductive seasonality on seminal quality. We hypothesised that seminal quality variations among whooping cranes and ejaculates within a given individual over time were due to bird age and stage of breeding season. In 2010, twenty-nine whooping cranes of 5 age groups housed at Patuxent Wildlife Research Center (Laurel, MD, USA) were studied: ≤5 years (n = 3); 6–10 years (n = 7); 11–15 years (n = 7); 16–20 years (n = 4); >20 years old (n = 8). Semen was collected using a manual manipulation technique at 3 stages of the breeding season: early (March, n = 29) mid (April, n = 24), and late (May, n = 14). Samples were evaluated for seminal volume and sperm concentration, motility, and morphology, with data evaluated by analysis of variance. Bird age had no influence on seminal quality, whereas stage of breeding season affected seminal volume and the proportion of sperm with normal morphology (95% confidence interval). Specifically, samples collected during Mid breeding season had the highest volume (mean ± SEM; early: 42.0 ± 8.0 μL; mid: 66.0 ± 15.2 μL; late: 39.7 ± 17.8 μL), but lowest proportions of structurally normal sperm (early: 78.4 ± 3.7%: mid: 61.5 ± 3.2%; late: 69.7 ± 3.4%). There was a significant difference (P = 0.06) in sperm concentration among stages of the breeding season (early: 66.3 ± 18.8 × 106 sperm mL–1; mid: 179.2 ± 46.2 × 106 sperm mL–1; late: 91.4 ± 47.8 × 106 sperm mL–1). Sperm motility was unaffected by season (early: 36.4 ± 3.5%; mid: 45.9 ± 4.1%; late: 48.0 ± 4.9%). In summary, there is a peak in seminal quality that corresponds with higher volume and more sperm during the mid stage of the season, although with higher instances of structural abnormalities. Despite the small founder base for this species, males in this population produce sperm with no variation in seminal quality across a wide variation in age.

Low genetic diversity in Polish populations of sibling ant species: Lasius niger (L.) and Lasius platythorax Seifert (Hymenoptera, Formicidae)

We present preliminary data on mitochondrial DNA diversity within and among populations of the ants Lasius niger and Lasius platythorax in Poland. Phylogenetic analysis based on the mitochondrial DNA markers: cytochrome c oxidase subunit I (cox1) and 16S ribosomal RNA (16S rRNA) confirms the species status of L. niger and L. platythorax. Intraspecific variability is low in both species, which might be a result of severe bottlenecks and rapid postglacial expansion into Central Europe.

An inexact interior point method for L 1-regularized sparse covariance selection

Sparse covariance selection problems can be formulated as log-determinant (log-det) semidefinite programming (SDP) problems with large numbers of linear constraints. Standard primal–dual interior-point methods that are based on solving the Schur complement equation would encounter severe computational bottlenecks if they are applied to solve these SDPs. In this paper, we consider a customized inexact primal–dual path-following interior-point algorithm for solving large scale log-det SDP problems arising from sparse covariance selection problems. Our inexact algorithm solves the large and ill-conditioned linear system of equations in each iteration by a preconditioned iterative solver. By exploiting the structures in sparse covariance selection problems, we are able to design highly effective preconditioners to efficiently solve the large and ill-conditioned linear systems. Numerical experiments on both synthetic and real covariance selection problems show that our algorithm is highly efficient and outperforms other existing algorithms.

The imprecision of heterozygosity-fitness correlations hinders the detection of inbreeding and inbreeding depression in a threatened species

In nonpedigreed wild populations, inbreeding depression is often quantified through the use of heterozygosity-fitness correlations (HFCs), based on molecular estimates of relatedness. Although such correlations are typically interpreted as evidence of inbreeding depression, by assuming that the marker heterozygosity is a proxy for genome-wide heterozygosity, theory predicts that these relationships should be difficult to detect. Until now, the vast majority of empirical research in this area has been performed on generally outbred, nonbottlenecked populations, but differences in population genetic processes may limit extrapolation of results to threatened populations. Here, we present an analysis of HFCs, and their implications for the interpretation of inbreeding, in a free-ranging pedigreed population of a bottlenecked species: the endangered takahe (Porphyrio hochstetteri). Pedigree-based inbreeding depression has already been detected in this species. Using 23 microsatellite loci, we observed only weak evidence of the expected relationship between multilocus heterozygosity and fitness at individual life-history stages (such as survival to hatching and fledging), and parameter estimates were imprecise (had high error). Furthermore, our molecular data set could not accurately predict the inbreeding status of individuals (as 'inbred' or 'outbred', determined from pedigrees), nor could we show that the observed HFCs were the result of genome-wide identity disequilibrium. These results may be attributed to high variance in heterozygosity within inbreeding classes. This study is an empirical example from a free-ranging endangered species, suggesting that even relatively large numbers (>20) of microsatellites may give poor precision for estimating individual genome-wide heterozygosity. We argue that pedigree methods remain the most effective method of quantifying inbreeding in wild populations, particularly those that have gone through severe bottlenecks.

Population Bottlenecks and Increased Hatching Failure in Endangered Birds

Severe population bottlenecks are expected to lead to increases in inbreeding depression and to reduce the long-term viability of populations. We compared hatching failure across 51 threatened bird species to test the relation between the size of population bottleneck and population viability. Bottleneck size was defined as the lowest population size recorded in a species. Hatching failure was estimated as the proportion of eggs that failed to hatch due to infertility and embryonic death, both of which increase with inbreeding. The size of the bottleneck varied from 4 to 20,000 individuals across species and had a significant negative effect on hatching failure, a pattern that was consistent when we controlled for the confounding effects of phylogeny, body size, clutch size, time since the bottleneck occurred, and latitude. Hatching failure varied from 3 to 64% across species and was more than 10% in all populations passing through bottlenecks below 100–150 individuals. Our results show that the negative consequences of bottlenecks on hatching success are widespread in the populations of species we examined, and emphasize the conservation benefit of preventing bottlenecks below 150 individuals.

Unexpected Island Effects at an Extreme: Reduced Y Chromosome and Mitochondrial DNA Diversity in Nias

The amount of genetic diversity in a population is determined by demographic and selection events in its history. Human populations which exhibit greatly reduced overall genetic diversity, presumably resulting from severe bottlenecks or founder events, are particularly interesting, not least because of their potential to serve as valuable resources for health studies. Here, we present an unexpected case, the human population of Nias Island in Indonesia, that exhibits severely reduced Y chromosome (non-recombining portion of the Y chromosome [NRY]) and to a lesser extent also reduced mitochondrial DNA (mtDNA) diversity as compared with most other populations from the Asia/Oceania region. Our genetic data, collected from more than 400 individuals from across the island, suggest a strong previously undetected bottleneck or founder event in the human population history of Nias, more pronounced for males than for females, followed by subsequent genetic isolation. Our findings are unexpected given the island's geographic proximity to the genetically highly diverse Southeast Asian world, as well as our previous knowledge about the human history of Nias. Furthermore, all NRY and virtually all mtDNA haplogroups observed in Nias can be attributed to the Austronesian expansion, in line with linguistic data, and in contrast with archaeological evidence for a pre-Austronesian occupation of Nias that, as we show here, left no significant genetic footprints in the contemporary population. Our work underlines the importance of human genetic diversity studies not only for a better understanding of human population history but also because of the potential relevance for genetic disease-mapping studies.

Genetic structure of the critically endangered plant Tricyrtis ishiiana (Convallariaceae) in relict populations of Japan

Tricyrtis ishiiana is a relic endemic plant taxon of the Convallariaceae that inhabits two nearby gorges in Kanagawa Prefecture, Japan. The distribution range and number of populations are thought to have been reduced to the present refugial populations during the Quaternary climatic oscillations. Because of its showy flowers, this plant has faced illegal removal from its natural habitats for horticultural use and has been designated a critically endangered species (class IA). In this study, we analyzed the genetic structure of the relict populations of T. ishiiana in order to contribute to the conservation strategies of the prefectural government. Our analyses of nine nuclear microsatellite loci detected high genetic diversity (HE = 0.704 and HO = 0.541) for the two populations. The two populations were slightly differentiated (RST = 0.032), accompanied by faint substructure across the populations (K = 3). In addition, each population exhibited spatial genetic structuring. The relatively low inbreeding coefficient for both populations together (FIS = 0.233) and each population separately (FIS = 0.217–0.246) may be attributable to crossing among descendants within a population along with occasional gene flow between the populations. These results suggested that the extant populations have not experienced a severe bottleneck. The two extant populations were genetically differentiated at a very low level, accompanied by occasional pollen flow via pollinators and/or seed dispersal by gravity in the mountainous environment. Occasional gene exchange between the populations has allowed T. ishiiana to harbor high genetic diversity despite being a relic plant confined to two small refugial populations.

Social complexity and linguistic diversity in the Austronesian and Bantu population expansions

Reconstructing the rise and fall of social complexity in human societies through time is fundamental for understanding some of the most important transformations in human history. Phylogenetic methods based on language diversity provide a means to reconstruct pre-historic events and model the transition rates of cultural change through time. We model and compare the evolution of social complexity in Austronesian (n = 88) and Bantu (n = 89) societies, two of the world's largest language families with societies representing a wide spectrum of social complexity. Our results show that in both language families, social complexity tends to build and decline in an incremental fashion, while the Austronesian phylogeny provides evidence for additional severe demographic bottlenecks. We suggest that the greater linguistic diversity of the Austronesian language family than Bantu likely follows the different biogeographic structure of the two regions. Cultural evolution in both the Bantu and Austronesian cases was not a simple linear process, but more of a wave-like process closely tied to the demography of expanding populations and the spatial structure of the colonized regions.

Population genetic structure of island and mainland populations of the quokka, Setonix brachyurus (Macropodidae): a comparison of AFLP and microsatellite markers

Translocation and reintroduction are important tools for the conservation or recovery of species threatened with extinction in the wild. However, an understanding of the potential genetic consequences of mixing populations requires an understanding of the genetic variation within, and similarities among, donor and recipient populations. Genetic diversity was measured using two independent marker systems (microsatellites and AFLPs) for one island and four small remnant mainland populations of Setonix brachyurus, a threatened medium sized macropod restricted to fragmented habitat remnants and two off-shore islands in southwest Australia. Microsatellite diversity in the island population (Rs = 3.2, He = 71%) was similar to, or greater than, all mainland populations (Rs = 2.1–3.9, He = 34-71%). In contrast, AFLP diversity was significantly lower in the island population (PPL = 20.5; Hj = 0.118) compared to all mainland populations (mean PPL = 79.5–89.7; mean Hj = 0.23–0.29). Microsatellites differentiated all (mainland and island) populations from each other. However, AFLP only differentiated the island population from the mainland populations—all mainland populations were not significantly differentiated from each other for this marker. Given a known time since isolation of the island population from the mainland (6,000 years ago), and an overall more conservative rate of evolution of AFLP markers, our results are consistent with mainland populations fragmenting thousands of years ago (but <6,000 years), probably as a consequence of reduced rainfall and the constriction of the preferred mesic habitat of quokkas. Our results also support a recent history of severe population bottlenecks in mainland populations, and a long history of bottlenecks of the island population, but reflect a recent explosion in numbers since European occupation of the island. Our results indicate that translocation of island populations to supplement mainland populations would introduce genetically markedly differentiated, and possibly maladapted, individuals.

Genetic signatures of population change in the British golden eagle (Aquila chrysaetos)

The golden eagle (Aquila chrysaetos) was once widely distributed in the uplands of the British Isles, but is now extinct in Ireland, and largely confined to the highlands and islands of Scotland. As the precise extent and severity of the reduction in population size are unclear, it is important to understand how the population was affected by the decline. We therefore genotyped 13 polymorphic microsatellite loci in 172 individuals from the contemporary British population and compared their genetic diversity to 70 British and 9 Irish museum specimens. Despite the recent population decline, there is only slight evidence for a concomitant loss of genetic variation. Instead, two likelihood-based Bayesian methods provided evidence for a severe ancient genetic bottleneck, possibly caused by the fragmentation of a large mainland European population and/or the founding effects of colonising the British Isles. As the population persisted despite this ancient bottleneck, our conclusion is that there is limited need for intervention to augment the present-day genetic diversity. The main short-term objective of conservation measures should be to increase population sizes by continuous safeguarding of individuals and habitat management. Finally, we also confirmed that, for management purposes, the species should be considered a single population unit and that the extinct Irish population was not differentiated from the British one.

China's Environmental Challenges and Implications for the World

After three decades of exceptional economic growth, China has become a global economic powerhouse. As the economy has grown, though, so have China's environmental challenges, causing enormous socioeconomic consequences for China and the rest of the world. The global financial crisis has prompted China to create more domestic demand for consumption and implement massive infrastructure construction. Although China has the second-largest total gross domestic product (GDP) in the world, its per capita GDP is still much lower than per capita GDP of developed countries: there is much room for further increase in GDP and consequent environmental challenges. Despite China's many efforts to protect the environment and improve resource use efficiency, increasing environmental pollution and resource scarcity have become a severe bottleneck for sustainable development. Because of China's size, these and other challenges and opportunities have huge implications for the world. However, literature related to China's various environmental challenges and rapid changes is scattered. In this article, we outline China's socioeconomic transformation, synthesize China's environmental challenges and their interrelationships, illustrate impacts of environmental challenges on human well-being in China and beyond, and offer a systems approach to addressing environmental sustainability.

Genetic load, inbreeding depression and heterosis in an age‐structured metapopulation

In a metapopulation, the process of recurrent local extinction and recolonization gives rise to an age structure among demes. Recently established demes will tend to differ from older demes in terms of the levels of genetic diversity found within them and the way this diversity is distributed among demes in the same and different ages. The effects of population turnover on average levels of genetic diversity among demes in a metapopulation have been the focus of much attention, both for neutral and nonneutral loci, but much less is known about the distribution of nonneutral genetic diversity among demes of different ages. In this paper, we used computer simulations to study the distribution of genetic load, inbreeding depression and heterosis in an age-structured metapopulation. We found that, for mildly deleterious mutations, within-deme inbreeding depression increased, whereas heterosis and genetic load decreased with deme age following severe colonization bottlenecks. In contrast, recessive lethal alleles tended to be purged during colonization, with older populations showing higher genetic load and higher within-deme inbreeding depression. Heterosis caused by recessive lethal alleles and resulting from gene flow among different demes tended to be greatest for young demes, because the mutations responsible tended to be purged in the first few generations after colonization, but its effects increased again as populations grow older as a result of immigration. Our results point to a need for estimates of genetic diversity, genetic load, within-deme inbreeding depression and heterosis in demes of different age classes separately.

Genes in evolution: the control of diversity and speciation

Genes in evolution: the control of diversity and speciation

Status of harbour seals (&lt;i&gt;Phoca vitulina&lt;/i&gt;) in the Baltic proper

The small population of harbour seals in the Baltic proper descend from seals that entered into the Baltic some 8,000 years ago. They form a genetically separate population with private alleles not present elsewhere. They were hunted close to extinction in the beginning of the 20th century and experienced a severe bottle-neck with perhaps only ten reproductive females in the 1970s. Protective measures and reduction of xenobiotic substances have improved the situation, and the hauled-out moulting population size was 588 in 2008, and about 100 pups have been born annually during the past few years. The protective measures in the form of banned hunting and establishment of protected areas will suffice to allow the population to grow, but the population will not reach favourable conservation status within foreseeable future.

Divergence, demography and gene loss along the human lineage

Genomic DNA sequences are an irreplaceable source for reconstructing the vanished past of living organisms. Based on updated sequence data, this paper summarizes our studies on species divergence time, ancient population size and functional loss of genes in the primate lineage leading to modern humans (Homo sapiens sapiens). The inter- and intraspecific comparisons of DNA sequences suggest that the human lineage experienced a rather severe bottleneck in the Middle Pleistocene, throughout which period the subdivided African population played a predominant role in shaping the genetic architecture of modern humans. Also, published and newly identified human-specific pseudogenes (HSPs) are enumerated in order to infer their significance for human evolution. Of the 121 candidate genes obtained, authentic HSPs turn out to comprise only 25 olfactory receptor genes, four T cell receptor genes and nine other genes. The fixation of HSPs has been too rare over the past 6–7 Myr to account for species differences between humans and chimpanzees.

Phylogeography of Cycas revoluta Thunb. (Cycadaceae) on the Ryukyu Islands: very low genetic diversity and geographical structure

Variations in the chloroplast and mitochondrial DNA of Cycas revoluta Thunb. (Cycadaceae) were examined in 22 populations distributed across the Ryukyu Islands and southern Kyushu. Among the 14,130 bp of sequence examined, only one site mutation and one indel were polymorphic. The identified polymorphisms were located in the spacers between trnS (UGA) and trnfM (CAU) of the chloroplast DNA and between nad1 exon B and exon C of the mitochondrial DNA, respectively. Three haplotypes were identified from the Ryukyu Islands and southern Kyushu. The areas of distribution of the three haplotypes were highly geographically structured. The boundaries of two of the three haplotypes were demarcated by Okinoerabujima Island in the middle Ryukyus. The northern type and southern types lay north and south of the island, respectively. The third haplotype was almost sympatrically distributed with the southern type. The genetic variation within C. revoluta was estimated to be very low (h = 0.641, π = 0.00071) in comparison to its relative in Taiwan, C. taitungensis, which possesses 97 cpDNA haplotypes and 55 mtDNA haplotypes from two relic populations. A reasonable explanation for the low genetic diversity of the cycad on the Ryukyu Islands could be severe bottleneck effects, resulting from the submersion of low islands and the diminished landmass of islands in the interglacial age in the Quaternary period. The geographically restricted nature of the haplotypes could be attributed to vicariance resulting from the land configuration of the Ryukyu Islands, including changes in geography during the interglacial age in the Quaternary.

Contrasting genetic variation and differentiation on Hainan Island and the Chinese mainland populations of Dacrycarpus imbricatus (Podocarpaceae)

Dacrycarpus imbricatus is a vulnerable conifer in China whose geographical distribution encompasses large island but small mainland populations, providing a framework for contrasting the patterns of population genetic composition. In this study, seven populations on Hainan Island and the Chinese mainland were sampled throughout its distribution range and assessed using ISSR. The results did not show significant differences neither in genetic variation nor in genetic differentiation between the island and the mainland populations ( P > 0.05). Severe bottlenecks were identified at population, island/mainland as well as range-wide scales. A relatively high level of variation but a low degree of differentiation was revealed. Ecological and life traits were suggested to play main roles in the shaping of genetic variation pattern. Of them long generation times could have exerted a lagging effect on both the genetic variation and differentiation. Our findings may contribute to establish management practices.

Origins, ages and population histories: comparative phylogeography of endemic Hawaiian butterflyfishes (genus Chaetodon)

AbstractAim To investigate phylogeographic relationships, genetic connectivity and potential colonization routes for Hawaii’s endemic butterflyfishes (family Chaetodontidae).Location The Hawaiian Archipelago (central Pacific Ocean).Methods Molecular genetic analysis of mitochondrial DNA from three species of endemic Hawaiian butterflyfishes (Chaetodon multicinctus, n = 280; Chaetodon miliaris, n = 408; Chaetodon fremblii, n = 358) sampled from across the Hawaiian Archipelago was used in a suite of population genetic analyses to examine population histories and calculate coalescence times. We review a recent phylogenetic hypothesis for the Chaetodontidae and optimize ancestral distributions to nodes as a means of inferring colonization pathways to Hawaii.Results We found no evidence for population subdivisions across their ranges for any of the three endemic Hawaiian butterflyfish species (ΦST ≈ 0; P &gt; 0.05 in each case). Coalescence analyses revealed that C. multicinctus, C. miliaris and C. fremblii date to genetic bottlenecks of c. 12 ka (95% confidence interval of τ, 0–46,732 years ago), c. 74 ka (95% confidence interval of τ, 62,918–105,699 years ago) and c. 301 ka (95% confidence interval of τ, 88,981–478,495 years ago), respectively. We found that the West Pacific appears to be the ancestral source for two of three independent colonization events to Hawaii (leading to the speciation of C. miliaris and C. fremblii). The third colonization of Hawaii (leading to the divergence of C. multicinctus) is ambiguous, but may have involved island‐hopping from the South Pacific via the Line Islands.Main conclusions Our results are consistent with the growing body of data indicating that ecological specialists may be more susceptible to severe population bottlenecks during large‐scale climatic variation on evolutionary time‐scales. The isolation of the Hawaiian Archipelago presents challenges for colonization by even the most highly dispersive marine organisms, and routes of colonization by endemic butterflyfishes show a variable pattern, indicating that there may be several pathways, both spatially and temporally, for marine fauna to colonize Hawaii. Hawaiian endemic butterflyfishes appear to represent genetically homogeneous populations across the archipelago.

Phylogeographic signatures of northward post‐glacial colonization from high‐latitude refugia: a case study of bank voles using museum specimens

There is mounting evidence that some European temperate species did not respond to the last (Weichselian) glaciation by simply shifting their distributions to the Mediterranean region but also survived at higher latitudes previously considered inhospitable. However, it remains to be determined to what extent such high-latitude glacial refugia contributed to post-glacial colonization of Europe. The bank vole Myodes glareolus apparently survived in a high-latitude glacial refugium in the Carpathian Mountains. Here, we used 144 new mitochondrial DNA sequences (largely obtained from museum skins), together with relevant previous data, to investigate whether the phylogeography of bank voles currently living in deglaciated areas north of the Carpathians reflects colonization from this or other refugia. Phylogenetic reconstruction resolved the newly identified haplotypes into three major clades. The majority of voles sampled in Poland carried haplotypes of the Carpathian clade, previously only known from the Carpathians and their immediate vicinity. Voles from eastern Poland and northern Germany carried haplotypes of the Eastern clade, also found in eastern Europe and Siberia, and six voles from scattered localities carried haplotypes of the Western clade, which has a west European distribution. Therefore, the results suggest the contribution of multiple glacial refugia. However, the occurrence of the Carpathian clade over a large area north of the Carpathians up to the Baltic Sea coast indicates a particular importance of the Carpathian refugium. Thus, a substantial involvement of a high-latitude refugium in the post-glacial colonization of Europe by bank voles is inferred. Likely as the consequence of the high-latitude survival, the Carpathian clade lacks evidence of the severe demographic bottleneck during the Last Glacial Maximum that is observed in the Eastern clade. The contact zone between the expanding populations of the Carpathian and Eastern clades coincides with subdivisions in other species and may represent a new post-glacial suture zone.