Meeting review: American Genetics Association Symposium on the genetics of speciation

Yeast can be engineered to carry human chromosomes; highly diverged ducks can produce viable, fertile offspring; and mitochondrial genes can move between widely divergent groups of plants. Some sunflower or oak species have porous genomes; mice, crickets, birds, and butterflies form hybrid zones; and bacterial lineages have been exchanging genes for several billion years. Even so, nature is discrete and full of species. Here, we discuss some of the ingredients that make nature discrete and can lead to clustering even in the presence of gene flow. Many of these results have been recently published, in this issue and elsewhere, and were discussed at the Genetics of Speciation Symposium held at the annual meeting of the American Genetics Association, Vancouver, Canada, in 2006.     

Maternal effect of a hybrid inviability gene in Tribolium castaneum

The Tribolium castaneum hybrid inviability gene, H, was selectively introgressed into a genetic background lacking H through serial paternal backcrosses. This revealed a poor viability phenotype (partial paralysis and poor control of the limbs, referred to as tremor) not present in the parent strains. Tremor cosegregated with H, but was expressed only when transmitted paternally and only when H was not also present maternally. The inferred maternal, self‐suppressive effect of H may explain nonreciprocal incompatibilty previously observed between H and H‐incompatible strains. This revised version was published online in July 2006 with corrections to the Cover Date.     

A test of alternative hypotheses for kin recognition in cannibalistic tiger salamanders

The function of kin recognition is controversial. We investigatedtheadaptive significance of kin discrimination in cannibalistictiger salamanderlarvae, Ambystoma tigrinum. Previous laboratoryexperiments show thatcannibals preferentially consume lessrelated individuals. We hypothesizedthat this example of kinrecognition (1) is a laboratory artifact, (2) is aby-productof sibship-specific variation in escape responses, becausecannibalsfrom families with rapid responses may be more likely to cannibalizeslowlyescaping non-kin, (3) is an epiphenomenon of species recognition,(4)functions in disease avoidance, because kin may be moreinfectious thannon-kin, or (5) is favored by kin selection.We evaluated these fivehypotheses by using laboratory and fieldexperiments to test specificpredictions made by each hypothesis.We rejected hypotheses 1-4 above because(1) kin recognitionwas expressed in the wild, (2) escape responses did notreliablypredict whether a cannibal would ingest kin or non-kin, (3)kinrecognition was not most pronounced in populations wheretiger salamandersco-occur with other species of salamanders,and (4) non-kin prey were morelikely than kin to transmit pathogensto cannibals. However, we establishedthat the necessary conditionfor kin selection, Hamilton's rule, was met.Thus, our resultsimplicate kin selection as the overriding reason thatcannibalistictiger salamanders discriminate kin.     

Contemporary hybrid speciation in sculpins (Cottus spp.)

Natural hybridization between closely related taxa is frequent in many organismal groups, yet it has long been perceived as a force preventing diversification and speciation, especially so in animals. In recent years, growing evidence in favour of hybridization facilitating adaptive divergence has accumulated ( Mallet 2007 ; Mavárez & Linares 2008 ; Nolte & Tautz 2010 ). Homoploid hybrid speciation (the formation of hybrid lineages without changes in chromosome number) occurs when distinct species come into contact, hybridize, and at least in part of their range, produce hybrid swarms. If the hybrid genotypes can then colonize areas of the adaptive landscape inaccessible to ancestral species, they may eventually form new distinct lineages, reproductively isolated from their ancestors. Invasive sculpins (Cottus sp.) are one of a few good examples of homoploid hybrid speciation in animals. In this issue, Stemshorn et al. (2011) identified three distinct hybrid lineages, which have emerged out of a secondary contact situation of Cottus rhenanus and Cottus perifretum. Hybrids have recently invaded large river habitats unsuitable to ancestral species. Through the use of genetic mapping, the authors established that contrary to expectations, chromosomal rearrangements were not apparent in the hybrid lineages. In addition, different population genetic models were tested and the results suggest that contemporary gene flow from ancestral species represents an important component of the system. As such, recent and ongoing hybridization appears to be promoting the appearance of phenotypes adapted to novel environments. The examination of partially isolated lineages such as invasive hybrid sculpins should permit to identify early adaptive genetic changes before they become confounded by differences arising once speciation is complete.     

Genetics and evolution of hybrid male sterility in house mice

Comparative genetic mapping provides insights into the evolution of the reproductive barriers that separate closely related species. This approach has been used to document the accumulation of reproductive incompatibilities over time, but has only been applied to a few taxa. House mice offer a powerful system to reconstruct the evolution of reproductive isolation between multiple subspecies pairs. However, studies of the primary reproductive barrier in house mice-hybrid male sterility-have been restricted to a single subspecies pair: Mus musculus musculus and Mus musculus domesticus. To provide a more complete characterization of reproductive isolation in house mice, we conducted an F(2) intercross between wild-derived inbred strains from Mus musculus castaneus and M. m. domesticus. We identified autosomal and X-linked QTL associated with a range of hybrid male sterility phenotypes, including testis weight, sperm density, and sperm morphology. The pseudoautosomal region (PAR) was strongly associated with hybrid sterility phenotypes when heterozygous. We compared QTL found in this cross with QTL identified in a previous F(2) intercross between M. m. musculus and M. m. domesticus and found three shared autosomal QTL. Most QTL were not shared, demonstrating that the genetic basis of hybrid male sterility largely differs between these closely related subspecies pairs. These results lay the groundwork for identifying genes responsible for the early stages of speciation in house mice.     

Population genetic analysis reveals a homoploid hybrid origin of Stephanomeria diegensis (Asteraceae)

Homoploid hybrid speciation has generally been viewed as a rare evolutionary phenomenon, with relatively few well-documented cases in nature. Here, we investigate the origin of Stephanomeria diegensis , a diploid flowering plant species that has been proposed to have arisen as a result of hybridization between S. exigua and S. virgata . Across the range of S. diegensis , all individuals share a common chloroplast haplotype with S. virgata while showing a greater affinity for S. exigua in terms of nuclear genetic diversity. A prinicipal coordinates analysis (PCO) based on the nuclear data revealed that S. diegensis is most similar to each parent along different axes. Moreover, a Bayesian clustering analysis as well as a hybrid index-based analysis showed evidence of mixed ancestry, with approximately two thirds of the S. diegensis nuclear genome derived from S. exigua . These results provide strong support for a homoploid hybrid origin of S. diegensis . Finally, contrary to the finding that homoploid hybrid species are typically multiply-derived, our results were most consistent with a single origin of this species.     

Haldane's rule in the 21st century

Haldane's Rule (HR), which states that 'when in the offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous (heterogametic) sex', is one of the most general patterns in speciation biology. We review the literature of the past 15 years and find that among the ～85 new studies, many consider taxa that traditionally have not been the focus for HR investigations. The new studies increased to nine, the number of 'phylogenetically independent' groups that comply with HR. They continue to support the dominance and faster-male theories as explanations for HR, although due to increased reliance on indirect data (from, for example, differential introgression of cytoplasmic versus chromosomal loci in natural hybrid zones) unambiguous novel results are rare. We further highlight how research on organisms with sex determination systems different from those traditionally considered may lead to more insight in the underlying causes of HR. In particular, haplodiploid organisms provide opportunities for testing specific predictions of the dominance and faster X chromosome theory, and we present new data that show that the faster-male component of HR is supported in hermaphrodites, suggesting that genes involved in male function may evolve faster than those expressed in the female function.     

Landscape genetics of alpine Sierra Nevada salamanders reveal extreme population subdivision in space and time

Quantifying the influence of the landscape on the genetic structure of natural populations remains an important empirical challenge, particularly for poorly studied, ecologically cryptic species. We conducted an extensive microsatellite analysis to examine the population genetics of the southern long‐toed salamander (Ambystoma macrodactylum sigillatum) in a naturally complex landscape. Using spatially explicit modelling, we investigated the influence of the Sierra Nevada topography on potential dispersal corridors between sampled populations. Our results indicate very high‐genetic divergence among populations, high within‐deme relatedness, and little evidence of recent migration or population admixture. We also discovered unexpectedly high between‐year genetic differentiation (F_ST) for breeding sites, suggesting that breeding groups vary over localized space and time. While environmental factors associated with high‐elevation montane habitats apparently play an important role in shaping population differentiation, additional, species‐specific biological processes must also be operating to account for observed deviations from temporal, among‐year panmixia. Our study emphasizes the population‐level insights that can be gained from high‐density sampling in space and time, and the highly substructured population biology that may characterize amphibians in extreme montane habitats.     

Analysis of a hybrid zone between subspecies of the tiger salamander (Ambystoma tigrinum) in central New Mexico,USA

We analyzed patterns of variation in polymorphic loci across a contact zone between two subspecies of tiger salamander, Ambystoma tigrinum nebulosum and A. t. mavortium, in west-central New Mexico. We found no fixed differences between A. t. mavortium and A. t. nebulosum. Allele frequencies across the contact zone did not vary concordantly among loci, but frequencies at two loci varied with elevation. Gene flow extends through the contact zone from A. t. mavortium into A. t. nebulosum, but not conversely. A. t. mavortium and A. t. nebulosum have no obvious impediments to gene flow within this contact zone, but some populations differ in time of reproduction. The contact zone comprises a variety of habitats, approximating typical A. t. mavortium or A. t. nebulosum habitats. There is an irregular pattern of differences in allelic frequencies among populations that covaries with habitats and is consistent with a model of a mosaic contact zone. Our results contrast with those of a study along the Front Range in Colorado, where allelic composition at some loci changed abruptly across a narrow zone of contact. These contrasting results suggest that the dynamics shaping the contact zone between the same taxa may differ. Absence of a similar pattern of genetic differentiation between A. t. mavortium and A. t. nebulosum in New Mexico and in Colorado suggests a complex set of evolutionary interactions along the eastern front of the Rocky Mountain axis.     

Secondary contact between Lycaeides idas and L. melissa in the Rocky Mountains: extensive admixture and a patchy hybrid zone

Studies of hybridization have increased our understanding of the nature of species boundaries, the process of speciation, and the effects of hybridization on the evolution of populations and species. In the present study we use genetic and morphological data to determine the outcome and consequences of secondary contact and hybridization between the butterfly species Lycaeides idas and L. melissa in the Rocky Mountains. Admixture proportions estimated from structure and geographical cline analysis indicate L. idas and L. melissa have hybridized extensively in the Rocky Mountains and that reproductive isolation was insufficient to prevent introgression for much of the genome. Geographical patterns of admixture suggest that hybridization between L. idas and L. melissa has led to the formation of a hybrid zone. The hybrid zone is relatively wide, given estimates of dispersal for Lycaeides butterflies, and does not show strong evidence of cline concordance among characters. We believe the structure of the Lycaeides hybrid zone might be best explained by the patchy distribution of Lycaeides, local extinction and colonization of habitat patches, environmental variation and weak overall selection against hybrids. We found no evidence that hybridization in the Rocky Mountains has resulted in the formation of independent hybrid species, in contrast to the outcome of hybridization between L. idas and L. melissa in the Sierra Nevada. Finally, our results suggest that differences in male morphology between L. idas and L. melissa might contribute to isolation, or perhaps even that selection has favoured the spread of L. melissa male genitalia alleles.     

Sexual isolation evolves faster than hybrid inviability in a diverse and sexually dimorphic genus of fish (Percidae: Etheostoma)

Abstract .Theory predicts that sexual (or behavioral) isolation will be the first form of reproductive isolation to evolve in lineages characterized by sexual selection. Here I directly compare the rate of evolution of sexual isolation with that of hybrid inviability in a diverse and sexually dimorphic genus of freshwater fish. The magnitude of both sexual isolation and hybrid inviability were quantified for multiple pairs of allopatric species. Rates of evolution were inferred by comparing genetic distances of these species pairs with the magnitude of each form of reproductive isolation: the slope of the regression of genetic distance on the magnitude of reproductive isolation represents the rate of evolution. Of the two forms of isolation, the magnitude of sexual isolation exhibited the steeper slope of regression, indicating that sexual isolation will tend to evolve to completion earlier than hybrid inviability, strictly as a by-product of evolution in geographically isolated populations. Additional evidence from the literature is used to qualitatively compare rates of evolution of sexual isolation with that of other forms of reproductive isolation. Preliminary comparisons support the prediction that sexual isolation will evolve more rapidly than other forms. Because Etheostoma is characterized by striking sexual dimorphism, these results are consistent with the hypothesis that sexual selection for exaggerated mate-recognition characters causes the relatively rapid evolution of sexual isolation.     

Constraints on speciation suggested by comparing lake-stream stickleback divergence across two continents

Adaptation to ecologically distinct environments can coincide with the emergence of reproductive barriers. The outcome of this process is highly variable and can range along a continuum from weak population differentiation all the way to complete, genome-wide divergence. The factors determining how far diverging taxa will move along this continuum remain poorly understood but are most profitably investigated in taxa under replicate divergence. Here, we explore determinants of progress towards speciation by comparing phenotypic and molecular divergence within young (<150 years) lake-stream stickleback pairs from Central Europe to divergence in older (thousands of years) archetypal lake-stream pairs from Vancouver Island, Canada. We generally find relatively weak divergence in most aspects of foraging morphology (gill raker number, body shape) in the European pairs, although substantial adaptive divergence is seen in gill raker length. Combined with striking overall phenotypic differences between the continents, this argues for genetic and time constraints on adaptive divergence in the European pairs. The European lake-stream pairs also do not display the strong habitat-related differentiation in neutral (microsatellite) markers seen in the Canadian watersheds. This indicates either the lack of strong reproductive barriers owing to weak adaptive divergence, or alternatively that neutral markers are poorly suited for detecting reproductive barriers if these emerge rapidly. Overall, our comparative approach suggests constraints on speciation due to genetic architecture and limited time for divergence. The relative importance of these factors remains to be quantified by future investigation.     

The contribution of the y chromosome to hybrid male sterility in house mice

Hybrid sterility in the heterogametic sex is a common feature of speciation in animals. In house mice, the contribution of the Mus musculus musculus X chromosome to hybrid male sterility is large. It is not known, however, whether F(1) male sterility is caused by X-Y or X-autosome incompatibilities or a combination of both. We investigated the contribution of the M. musculus domesticus Y chromosome to hybrid male sterility in a cross between wild-derived strains in which males with a M. m. musculus X chromosome and M. m. domesticus Y chromosome are partially sterile, while males from the reciprocal cross are reproductively normal. We used eight X introgression lines to combine different X chromosome genotypes with different Y chromosomes on an F(1) autosomal background, and we measured a suite of male reproductive traits. Reproductive deficits were observed in most F(1) males, regardless of Y chromosome genotype. Nonetheless, we found evidence for a negative interaction between the M. m. domesticus Y and an interval on the M. m. musculus X that resulted in abnormal sperm morphology. Therefore, although F(1) male sterility appears to be caused mainly by X-autosome incompatibilities, X-Y incompatibilities contribute to some aspects of sterility.     

Biomass export of salamanders and anurans from ponds is affected differentially by changes in canopy cover

1. Previous research shows that canopy‐associated shifts from an algal to a detritus‐based food web can affect anuran tadpoles negatively. This may not be true of salamander larvae, however, because they are predators. 2. To investigate the influence of canopy cover on the survival and growth of salamanders, and on the subsequent export of biomass from ponds, we conducted a mesocosm experiment examining effects of shading (high or low) and litter (leaves or grass) on Ambystoma maculatum (a forest specialist) and A. texanum (a habitat generalist). Additionally, we reanalysed data from Williams, Rittenhouse & Semlitsch (2008) to examine the effects of shading and litter on biomass export of three anurans: Rana sphenocephala, Pseudacris crucifer and Hyla versicolor. 3. In contrast to previous studies, we found that salamanders performed better in mesocosms with the characteristics of closed canopy ponds (high shade and leaf litter), which resulted in a greater export of biomass. Salamanders grew larger under closed canopy conditions, probably because of differences in prey abundance among treatments. Anurans responded differently to canopy cover than caudates. The biomass export of R. sphenocephala and P. crucifer was reduced under closed canopy conditions (although differently affected by litter and shading), while the biomass of H. versicolor was not affected. 4. This and other studies suggest that changes in canopy cover may induce a shift in the amphibians emerging from ponds, from primarily anurans in open canopy ponds to primarily salamanders in closed canopy ponds. Additional multispecies studies will determine whether these trends hold true for more diverse amphibian assemblages. Further investigation into the effects of canopy cover on salamanders will be important for understanding aquatic–terrestrial linkages.     

Isolation and characterization of microsatellite markers in the invasive shrub Mahonia aquifolium (Berberidaceae) and their applicability in related species

Microsatellite loci were isolated from a Mahonia aquifolium cultivar. We describe the variability of 10 loci in invasive European and native North American M. aquifolium and their transspecies amplification in native Mahonia repens and Mahonia pinnata from North America and one species of the related genus Berberis (Berberis vulgaris), native to Europe. The markers should be useful to reveal the genetic origin of invasive Mahonia populations and differences in the genetic make up between invasive and native populations.     

国家自然科学基金资助的生物入侵基础研究概况

基于1999~2010年国家自然科学基金资助项目,分析了我国生物入侵基础研究概况。在这期间,生物入侵领域得到资助的项目数和经费均呈现快速上升的趋势,资助的项目从1999年的3个增加到2010年的69个,资助的经费从1999年的94万元增加到2010年的1838万元。得到资助的项目数在不同学科的分布不均匀,其中,植物保护学科得到资助的项目数为123个,生态学科得到资助的项目数为82个,这2个学科得到资助的项目数占总项目数的67.9%,得到资助的经费占总经费的66.3%。资助项目的主要研究内容涉及22种入侵植物病原微生物、26种入侵动物和24种入侵植物,从中可以透视本领域的研究重点。资助的项目主要集中在华北、华东和华南地区的国家级科研机构和高等院校,这种区域分布格局与我国入侵生物的地理分布格局相吻合。为了进一步推动国家自然科学基金对生物入侵领域各项工作的资助,本文提出了一些合理化的建议。     

Molecular evidence for historical and recent population size reductions of tiger salamanders (Ambystoma tigrinum) in Yellowstone National Park

Population declines caused by natural and anthropogenic factors can quickly erode genetic diversity in natural populations. In this study, we examined genetic variation within 10 tiger salamander populations across northern Yellowstone National Park in Wyoming and Montana, USA using eight microsatellite loci. We tested for the genetic signature of population decline using heterozygosity excess, shifts in allele frequencies, and low ratios of allelic number to allelic size range (M-ratios). We found different results among the three tests. All 10 populations had low M-ratios, five had shifts in allele frequencies and only two had significant heterozygosity excesses. These results support theoretical expectations of different temporal signatures among bottleneck tests and suggest that both historical fish stocking, recent, sustained drought, and possibly an emerging amphibian disease have contributed to declines in effective population size.     

Differential timing of gene expression regulation between leptocephali of the two Anguilla eel species in the Sargasso Sea

The unique life-history characteristics of North Atlantic catadromous eels have long intrigued evolutionary biologists, especially with respect to mechanisms that could explain their persistence as two ecologically very similar but reproductively and geographically distinct species. Differential developmental schedules during young larval stages have commonly been hypothesized to represent such a key mechanism. We performed a comparative analysis of gene expression by means of microarray experiments with American and European eel leptocephali collected in the Sargasso Sea in order to test the alternative hypotheses of (1) differential timing of gene expression regulation during early development versus (2) species-specific differences in expression of particular genes. Our results provide much stronger support for the former hypothesis since no gene showed consistent significant differences in expression levels between the two species. In contrast, 146 genes showed differential timings of expression between species, although the observed expression level differences between the species were generally small. Consequently, species-specific gene expression regulation seems to play a minor role in species differentiation. Overall, these results show that the basis of the early developmental divergence between the American and European eel is probably influenced by differences in the timing of gene expression regulation for genes involved in a large array of biological functions.