Butterfly genomics sheds light on the process of hybrid speciation

How common is hybridization between species and what effect does it have on the evolutionary process? Can hybridization generate new species and what indeed is a species? In this issue, Gompert et al. (2014) show how massive, genome‐scale data sets can be used to shed light on these questions. They focus on the Lycaeides butterflies, and in particular, several populations from the western USA, which have characteristics suggesting that they may contain hybrids of two or more different species (Gompert et al. 2006). They demonstrate that these populations do contain mosaic genomes made up of components from different parental species. However, this appears to have been largely driven by historical admixture, with more recent processes appearing to be isolating the populations from each other. Therefore, these populations are on their way to becoming distinct species (if they are not already) but have arisen following extensive hybridization between other distinct populations or species (Fig.  1 ).

Figure 1 Open in figure viewer PowerPoint There has been extensive historical admixture between Lycaeides species with some new species arising from hybrid populations. (Photo credits: Lauren Lucas, Chris Nice, and James Fordyce).

Their data set must be one of the largest outside of humans, with over one and half thousand butterflies genotyped at over 45 thousand variable nucleotide positions. It is this sheer amount of data that has allowed the researchers to distinguish between historical and more recent evolutionary and demographic processes. This is because it has allowed them to partition the data into common and rare genetic variants and perform separate analyses on these. Common genetic variants are likely to be older while rare variants are more likely to be due to recent mutations. Therefore, by splitting the genetic variation into these components, the researchers were able to show more admixture among common variants, while rare variants showed less admixture and clear separation of the populations. The extensive geographic sampling of individuals, including overlapping distributions of several of the putative species, also allowed the authors to rule out the possibility that the separation of the populations was simply due to geographical distance. The authors have developed a new programme for detecting population structure and admixture, which does the same job as STRUCTURE (Pritchard et al. 2000 ), identifying genetically distinct populations and admixture between these populations, but is designed to be used with next generation sequence data. They use the output of this model for another promising new method to distinguish between contemporary and historical admixtures. They fixed the number of source populations in the model at two and estimated the proportion of each individual's genome coming from these two populations. Therefore, an individual can either be purely population 1, or population 2 or some mixture of the two (they call this value q, the same parameter exists in STRUCTURE). They then compared this to the level of heterozygosity coming from the two source populations in the individual's genome. If an individual is an F1 hybrid of two source populations, then it would have a q of 0.5 and also be heterozygous at all loci that distinguish the parental populations. On the other hand, if it is a member of a stable hybrid lineage, it might also have a q of 0.5 but would not be expected to be heterozygous at these loci, because over time the population would become fixed for one or other of the source population states either by drift or selection (Fig.  2 ). This is indeed what they find in the hybrid populations. They tend to have intermediate q values, but the level of heterozygosity coming from the source populations (which they call Q₁₂) was consistently lower than expected.

Figure 2 Open in figure viewer PowerPoint The Q‐matrix analysis used by Gompert et al. ( 2014 ) to distinguish between contemporary (hybrid swarm) and historical (stable hybrid lineage) admixture.

Overall, the results support several of the populations as being stable hybrid lineages. Nevertheless, the strictest definitions of hybrid species specify that the process of hybridization between the parental species must be instrumental in driving the reproductive isolation of the new species from both parental populations (Abbott et al. 2013 ). This is extremely hard to demonstrate conclusively because it requires us to first of all identify the isolating mechanisms that operated in the early evolution of the species and then to show that these were caused by the hybridization event itself. One advantage of the Lycaeides system is that the species appear to be in the early stages of divergence, so barriers to gene flow that are operating currently are likely to be those that are driving the species divergence. While there is some evidence that hybridization gave rise to traits that allowed the new populations to colonize new environments (Gompert et al. 2006 ; Lucas et al. 2008 ), there is clearly further work to be carried out in this direction. One of the rare examples of homoploid hybrid speciation (hybrid speciation without a change in chromosome number) where the reproductive isolation criterion has been demonstrated, comes from the Heliconius butterflies. In this case, hybridization of two species has been shown to give rise to a new colour pattern that instantly becomes reproductively isolated from the parental species due to mate preference for that pattern (Mavárez et al. 2006 ). However, while this has become a widely accepted example (Abbott et al. 2013 ), the naturally occurring ‘hybrid species’ in fact has derived most of its genome from one of the parental species, with largely just the colour pattern controlling locus coming from the other parent, a process that has been termed ‘hybrid trait speciation’ (Salazar et al. 2010 ). This distinction is an important one in terms of our understanding of the organization of biological diversity. While hybrid trait speciation will still largely fit the model of a neatly branching evolutionary tree, with perhaps only the region surrounding the single introgressed gene deviating from this model, hybrid species that end up with mosaic genomes, like Lycaeides, will not fit this model when considering the genome as a whole. This distinction also more broadly applies when comparing the patterns of divergence between Heliconius and Lycaeides. These two butterfly genera have been driving forward our understanding of the prevalence and importance of hybridization at the genomic level, but they reveal different ways in which hybridization can influence the organization of biological diversity. Recent work in Heliconius has shown that admixture is extensive and has been ongoing over a large portion of the evolutionary history of species (Martin et al. 2013 ; Nadeau et al. 2013 ). Nevertheless, this has not obscured the clear and robust pattern of a bifurcating evolutionary tree when considering the genome as a whole (Nadeau et al. 2013 ). In contrast in Lycaeides, the genome‐wide phylogeny clearly does not fit a bifurcating tree, resembling more of a messy shrub, with hybrid taxa falling at intermediate positions on the phylogeny (Gompert et al. 2014 ). The extent to which we need to rethink the way we describe and organize biological diversity will depend on the relative prevalence of these different outcomes of hybridization. We are likely to see many more of these types of large sequence data sets for ecologically interesting organisms. Gompert et al. ( 2014 ) show that these data need not only be a quantitative advance, but can also qualitatively change our understanding of the evolutionary history of these organisms. In particular, analysing common and rare genetic variants separately may provide information that would otherwise be missed. The emerging field of ‘speciation genomics’ (Seehausen et al. 2014 ) should follow this lead in developing new ways of making the most of the flood of genomic data that is being generated, but also improve methods for integrating this with field observations and experiments to identify the sources and targets of selection and divergence.

References

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This article was written and figures prepared by N.N. except as specified in the text (photo credits).

Citing Literature

Number of times cited according to CrossRef: 4

• V. Alex Sotola, David S. Ruppel, Timothy H. Bonner, Chris C. Nice, Noland H. Martin, Asymmetric introgression between fishes in the Red River basin of Texas is associated with variation in water quality, Ecology and Evolution, 10.1002/ece3.4901, 9 , 4, (2083-2095), (2019). Wiley Online Library
• Matej Bocek, Dominik Kusy, Michal Motyka, Ladislav Bocak, Persistence of multiple patterns and intraspecific polymorphism in multi-species Müllerian communities of net-winged beetles, Frontiers in Zoology, 10.1186/s12983-019-0335-8, 16 , 1, (2019). Crossref
• Nicola J. Nadeau, Takeshi Kawakami, Population Genomics of Speciation and Admixture, , 10.1007/13836_2018_24, (2018). Crossref
• Amanda Roe, Julian Dupuis, Felix Sperling, Molecular Dimensions of Insect Taxonomy in the Genomics Era, Insect Biodiversity, 10.1002/9781118945568, (547-573), (2017). Wiley Online Library

Volume 23 , Issue 18 September 2014

Pages 4441-4443     

Breeding density,habitat selection and reproductive rates of the Peregrine Falcon Falco peregrinus in Álava (northern Spain)

A population of 33–35 pairs of Peregrine Falcon in álava (north Spain) was studied with the aim of assessing the habitat attributes that influence breeding density, habitat selection and breeding success. A strong relationship was found between density of the species in each UTM (Universal Transverse Mercator) square of 10 × 10 km and cliff availability. Habitat selection was analysed by comparing 15 variables in 33 occupied and 25 unoccupied cliffs located at least 2 km from the nearest Peregrine pair. Significant differences were found in five variables: cliff dominance, distance to the nearest Golden Eagle Aquila chrysaetos nesting cliff, steepness and altitude (all showing larger values in occupied cliffs), and cliff orientation, with occupied cliffs facing preferably south and east. Orientation, dominance and distance to the nearest Golden Eagle pair, and the distance to the nearest Eagle Owl Bubo bubo nesting cliff, were included in a discriminant analysis which classified 82.76% of the cliffs correctly. The productivity of the studied population was 1.44 young/territorial pair (n = 45), and no consistent relationship was found between breeding success and habitat variables.     

Behavioral genomics and the study of speciation at a porous species boundary

Porous species boundaries are characterized by differential gene flow, where some regions of the genome experience divergent evolution while others experience the homogenizing effects of gene flow. If species can arise or remain distinct despite gene flow between them, speciation can only be understood on a gene by gene level. To understand the genetics of speciation, we therefore must identify the targets of selection that cause divergent evolution and identify the genetic architecture underlying such “speciation phenotypes”. This will enable characterization of genomic regions that are “free to flow” between species, and those that diverge in the face of gene flow. We discuss this problem in the genus Laupala, a morphologically cryptic, flightless group of crickets that has radiated in Hawaii. Because songs are used in courtship and always distinguish close relatives of Laupala as well as species in sympatry, we argue that songs in Laupala are speciation phenotypes. Here, we present our approaches to identify the underlying genomic regions and song genes that differentiate closely related species. We discuss what is known about the genetic basis of this species difference derived from classic quantitative genetics and quantitative trait locus mapping experiments. We also present a model of the molecular expression of cricket song to assist in our goal to identify the genes involved in song variation. As most species are sympatric and exchange genes with congeners, we discuss the importance of understanding the genetic and genomic architecture of song as a speciation phenotype that must be characterized to identify differential patterns of gene flow at porous species boundaries.     

Successful breeding attempt of a pair of Philippine tarsier (Tarsius syrichta) in a conservation center in Bilar,Bohol, Philippines and recommendations for tarsier husbandry

The Philippine tarsier (Tarsius syrichta) belongs to the least known nocturnal primates. Tarsiers and remaining biodiversity of the Philippines are under tremendous threats from increasing human expansion, with habitat loss and illegal pet trade being the main reasons for tarsier population decline. In addition, even though the attempts were made by western and local facilities, tarsiers have not survived well in captivity. In this paper, I present an example of successful breeding of the Philippine tarsier in captive conditions but in natural climate. As the most important elements of success, I see a large amount of space provided to tarsiers, the climate similar to their natural habitat and the food resembling their natural diet. Our pair of tarsiers were joined during the mating period and held separately outside the mating period, which corresponds with their behavior in the wild and may have played a crucial role in breeding success. Eliminating stress to animals is also important. The study can provide valuable guidelines for other facilities keeping tarsiers in the Philippines and help to improve tarsiers’ welfare and in the future help to establish a viable captive population of the Philippine tarsier that will serve as a backup population and also will decrease demand on tarsiers captured from the wild.     

新疆拟游隼生态观察

拟游隼（Falco pelegrinoides babylonicus)在国内仅见于新疆南部,作者于2001年4-6月在木扎特河流域对其繁殖进行了观察,窝雏数为3只,每日有5-6次喂食,食物以鸽类为主。     

Integrating population genetics and conservation biology in the era of genomics

As one of the final activities of the ESF-CONGEN Networking programme, a conference entitled ‘Integrating Population Genetics and Conservation Biology’ was held at Trondheim, Norway, from 23 to 26 May 2009. Conference speakers and poster presenters gave a display of the state-of-the-art developments in the field of conservation genetics. Over the five-year running period of the successful ESF-CONGEN Networking programme, much progress has been made in theoretical approaches, basic research on inbreeding depression and other genetic processes associated with habitat fragmentation and conservation issues, and with applying principles of conservation genetics in the conservation of many species. Future perspectives were also discussed in the conference, and it was concluded that conservation genetics is evolving into conservation genomics, while at the same time basic and applied research on threatened species and populations from a population genetic point of view continues to be emphasized.     

The genomics of adaptation,divergence and speciation: a congealing theory

In this issue, Flaxman et al. ( 2014 ) report the results of sophisticated whole‐genome simulations of speciation with gene flow, enhancing our understanding of the process by building on previous single‐locus, multilocus and analytical works. Their findings provide us with new insights about how genomes can diverge and the importance of statistical and chromosomal linkage in facilitating reproductive isolation. The authors characterize the conditions under which, even with high gene flow and weak divergent selection, reproductive isolation between populations can occur due to the emergent stochastic process of genomewide congealing, where numerous statistically or physically linked loci of small effect allow selection to limit effective migration rates. The initial congealing event can occur within a broad range conditions, and once initiated, the self‐reinforcing process leads to rapid divergence and ultimately two reproductively isolated populations. Flaxman et al.'s ( 2014 ) work is a valuable contribution to our understanding of speciation with gene flow and in making a more predictive field of evolutionary genomics and speciation.     

Maxent modeling for predicting the spatial distribution of three raptors in the Sanjiangyuan National Park,China

Upland buzzard (Buteo hemilasius), Saker falcon (Falco cherrug), and Himalayan vulture (Gyps himalayensis) are three common large raptors in the Sanjiangyuan National Park (SNP), China's first national park. Among them, Upland buzzard and Saker falcon play a significant role in controlling plateau rodent populations and reducing the transmission of pathogens carried by rodents. The Himalayan vulture can provide services for the redistribution and recycling of nutrients in the ecosystem, and play an irreplaceable role in the celestial burial culture of Tibetans in China. Exploring their habitat suitability is important for the protection of the three raptors. Our research was based on the current distribution of Upland buzzard, Saker falcon, and Himalayan vulture that we had extensively surveyed in the Sanjiangyuan National Park from 2016 to 2017. Combined with the correlation analysis of environmental variables, we utilized maximum entropy model (MaxEnt) to evaluate and compare the habitat suitability of the three species in the Sanjiangyuan National Park. Elevation, climate, and human disturbance factors, which had direct or indirect effects on species survival and reproduction, were all included in the model. Among them, elevation was the most important environmental variables affecting the suitability of habitats of three species. Temperature‐related factor was another important predictor. The high (>60%) suitable habitat areas for Upland buzzard, Saker falcon, and Himalayan vulture were 73,017.63, 40,732.78, and 61,654.33 km², respectively, accounted for 59.32%, 33.09%, and 50.08% of the Sanjiangyuan National Park and their total suitable area (i.e., the sum area of high and moderate habitats) reached 96.07%, 60.59%, and 93.70%, respectively. Besides, the three species have overlapping areas for the suitable habitats, which means that overlapping areas should be highly valued and protected. Therefore, understanding the distribution of suitable habitats of the three raptors can provide useful information and reasonable reference for us to put forward suggestions for their protection and regional management.     

Ribosomal DNAs: an exception to the conservation of gene order in rice genomes

rDNA (18S-5.8S-25S rDNA) and 5S rDNA loci were visualized on the chromosomes of six species of the genus Oryza by fluorescence in situ hybridization (FISH) and the labeled rice chromosomes were identified based on their condensation patterns. As a result, the chromosomes harboring rDNA and/or 5S rDNA loci were determined in the complement for all the known rice genomes. Variation in the location of the rDNA loci indicated the transpositional nature of the rDNAs in the genus Oryza, as also suggested in Triticeae and Allium. Comparative analysis of the locations of rDNA loci among rice, maize and wheat revealed that variability in the physical location of the rDNA loci was characteristic of the genus Oryza and also of the genera of Gramineae. This variability in the location of the rDNA loci between evolutionarily related species is in sharp contrast to the conservation of the general order of genes in their genomes.     

棕黑锦蛇的研究概况及保护问题

本文对棕黑锦蛇（Elaphe schrenckii）进行分类学等研究,棕黑锦蛇被认为包含两个亚种：指名亚种（Elaphe s.schrenckii）和赤峰亚种（Elaphe s.anomala）,但也有学者将后者提升为种,即赤峰锦蛇（Elaphe anomala）.有关该种分类问题,仍需要进一步综合考虑形态学和分子系统学分类研究.作为我国东北和华北地区体形最大的蛇种,棕黑锦蛇具有重要的生态和经济价值,但目前对其生物学特性和生态学研究极为有限,人工驯养繁育技术不成熟,过度利用导致野外种群遭到严重破坏.建议加强棕黑锦蛇生态学和人工繁育技术的研究,为有效保护和可持续利用提供科学依据.     

Captive breeding of squirrel monkeys,Saimiri sciureus and Saimiri boliviensis: The problem of hybrid groups

The electrophoretic variability of blood proteins coding for up to 32 genetic loci was analyzed in 108 squirrel monkeys (Saimiri sciureus, Saimiri boliviensis, hybrids) from two captive colonies. Twelve polymorphic loci with 31 alleles are reported. The biallelic Ada* locus, G-statistics and Hardy-Weinberg genotype equilibria are useful for recognizing hybrids between S. sciureus and S. boliviensis. Backcrosses in hybrid stocks and gene flow in a natural hybrid belt, however, complicate the taxonomic diagnosis of captive specimens: S. sciureus phenotypes imported from Peru possessed the allele Ada*132, which generally characterizes S. boliviensis (or species hybrids). The complex taxonomy of Saimiri spp. Requires careful planning of captive breeding. We suggest a genetic analysis of the founder individuals before their inclusion in the European studbook population and to breed S. sciureus from Guyana separately from Peruvian imports, because the latter bear a greater risk of being taxonomically heterogeneous. Zoo Biol 17:95–109, 1998. © 1998 Wiley-Liss, Inc.     

The relevance of pedigrees in the conservation genomics era

Over the past 50 years conservation genetics has developed a substantive toolbox to inform species management. One of the most long-standing tools available to manage genetics—the pedigree—has been widely used to characterize diversity and maximize evolutionary potential in threatened populations. Now, with the ability to use high throughput sequencing to estimate relatedness, inbreeding, and genome-wide functional diversity, some have asked whether it is warranted for conservation biologists to continue collecting and collating pedigrees for species management. In this perspective, we argue that pedigrees remain a relevant tool, and when combined with genomic data, create an invaluable resource for conservation genomic management. Genomic data can address pedigree pitfalls (e.g., founder relatedness, missing data, uncertainty), and in return robust pedigrees allow for more nuanced research design, including well-informed sampling strategies and quantitative analyses (e.g., heritability, linkage) to better inform genomic inquiry. We further contend that building and maintaining pedigrees provides an opportunity to strengthen trusted relationships among conservation researchers, practitioners, Indigenous Peoples, and Local Communities.     

Population genomics of sexual and asexual lineages in fissiparous ribbon worms (Lineus,Nemertea): hybridization,polyploidy and the Meselson effect

Comparative population genetics in asexual vs. sexual species offers the opportunity to investigate the impact of asexuality on genome evolution. Here, we analyse coding sequence polymorphism and divergence patterns in the fascinating Lineus ribbon worms, a group of marine, carnivorous nemerteans with unusual regeneration abilities, and in which asexual reproduction by fissiparity is documented. The population genomics of the fissiparous L. pseudolacteus is characterized by an extremely high level of heterozygosity and unexpectedly elevated π_N/π_S ratio, in apparent agreement with theoretical expectations under clonal evolution. Analysis of among‐species allele sharing and read‐count distribution, however, reveals that L. pseudolacteus is a triploid hybrid between Atlantic populations of L. sanguineus and L. lacteus. We model and quantify the relative impact of hybridity, polyploidy and asexuality on molecular variation patterns in L. pseudolacteus and conclude that (i) the peculiarities of L. pseudolacteus population genomics result in the first place from hybridization and (ii) the accumulation of new mutations through the Meselson effect is more than compensated by processes of heterozygosity erosion, such as gene conversion or gene copy loss. This study illustrates the complexity of the evolutionary processes associated with asexuality and identifies L. pseudolacteus as a promising model to study the first steps of polyploid genome evolution in an asexual context.     

Plenty more fish in the sea: comparative and functional genomics using teleost models.

Biology has collaborated with evolution to create an enormous repertoire of animal variation. This in turn has provided experimental biologists with models that can be used in the lab to simulate more complex systems. Amongst the organisms that have been used in this way are fish, where a large number of species have been utilised in a variety of different ways. Fish possess the smallest genomes of any vertebrate, making them ideal as models for genome analysis and gene discovery. Fish are also easy to maintain in a laboratory environment and can be bred easily. Fish often have well-defined physiology and respond well to many experimental procedures. Finally, fish are of great economic importance in their own right, as one of the world's largest sources of protein. In this review, the relationship between fish species is examined along with the role of different fish models in a wide range of biological disciplines.     

Progress in TILLING as a tool for functional genomics and improvement of crops

Food security is a global concern and substantial yield increases in crops are required to feed the growing world population. Mutagenesis is an important tool in crop improvement and is free of the regulatory restrictions imposed on genetically modified organisms. Targeting Induced Local Lesions in Genomes(TILLING), which combines traditional chemical mutagenesis with high‐throughput genome‐wide screening for point mutations in desired genes, offers a powerful way to create novel mutant alleles for both functional genomics and improvement of crops. TILLING is generally applicable to genomes whether small or large, diploid or evenallohexaploid, and shows great potential to address the major challenge of linking sequence information to the function of genes and to modulate key traits for plant breeding. TILLING has been successfully applied in many crop species and recent progress in TILLING is summarized below, especially on the developments in mutation detection technology, application of TILLING in gene functional studies and crop breeding. The potential of TILLING/EcoTILLING for functional genetics and crop improvement is also discussed. Furthermore, a small‐scale forward strategy including backcross and selfing was conducted to release the potential mutant phenotypes masked in M2(or M3) plants.     

Progress in TILLING as a tool for functional genomics and improvement of crops

Food security is a global concern and substantial yield increases in crops are required to feed the growing world population. Mutagenesis is an important tool in crop improvement and is free of the regulatory restrictions imposed on genetically modified organisms. Targeting Induced Local Lesions in Genomes（TILLING）, which combines traditional chemical mutagenesis with high‐throughput genome‐wide screening for point mutations in desired genes, offers a powerful way to create novel mutant alleles for both functional genomics and improvement of crops. TILLING is generally applicable to genomes whether small or large, diploid or evenallohexaploid, and shows great potential to address the major challenge of linking sequence information to the function of genes and to modulate key traits for plant breeding. TILLING has been successfully applied in many crop species and recent progress in TILLING is summarized below, especially on the developments in mutation detection technology, application of TILLING in gene functional studies and crop breeding. The potential of TILLING/EcoTILLING for functional genetics and crop improvement is also discussed. Furthermore, a small‐scale forward strategy including backcross and selfing was conducted to release the potential mutant phenotypes masked in M2（or M3） plants.     

Hormonal induction of spermiation,courting behavior and spawning in the southern bell frog,Litoria raniformis

We trialled the efficacy of various exogenous hormones to induce spermiation, courtship behavior, and spawning in the “endangered” southern bell frog, Litoria raniformis. Intralymphatic administration of Lucrin^®, a synthetic nonapeptide luteinizing hormone releasing hormone (LHRH), was used successfully to induce courting behaviors and ejaculation of spermatozoa in males. Various hormones, including Lucrin^®, another synthetic LHRH analog ([des‐Gly¹⁰, D‐Ala⁶]‐LHRH), human chorionic gonadotropin, progesterone, and a dopamine receptor antagonist failed to promote oviposition and spawning in females. This and earlier studies indicate that in the efficacy of hormonal induction in amphibians varies between taxa, hormones, and genders. The lack of response in females may limit the use of reproduction technology in the southern bell frog and closely related species of Australian bell frogs. Zoo Biol 29:774–782, 2010. © 2010 Wiley‐Liss, Inc.