The Drosophila Serido Speciation Puzzle: Putting New Pieces Together

The D. seridosuperspecies is a complex mosaic of populations distributed over a vast part of South America and showing various degrees of genetical divergence. We have analyzed its chromosomal constitution in 16 new localities of southeastern and southern Brazil. Both the metaphase and salivary gland chromosomes show a sharp split of these populations in two groups. Four populations, fixed for inversion 2e ⁸and showing the type I karyotype, represent the southwestern limit of D. seridotype B, which inhabits the Cerrado in central-western Brazil. The remaining populations are homozygous for 2x ⁷, an inversion also fixed in the Caatinga populations of northeastern Brazil. However, their karyotype, in those populations analyzed, belong to a different type (V) from that of the Caatinga populations. Populations in this second group are polymorphic for five inversions on chromosome 2 plus another on chromosome 5 and show considerable interpopulation differentiation. The breakpoints of chromosome 2 inversions are described and the inversion loops of several heterokaryotypes are presented. Biogeographical information suggests that there are clear ecological differences between the two groups of populations as well as among the populations within the second group. The possible role of host plants in promoting the genetic divergence among the D. seridopopulations is discussed. This revised version was published online in July 2006 with corrections to the Cover Date.     

Genomics of Secondarily Temperate Adaptation in the Only Non-Antarctic Icefish

White-blooded Antarctic icefishes, a family within the adaptive radiation of Antarctic notothenioid fishes, are an example of extreme biological specialization to both the chronic cold of the Southern Ocean and life without hemoglobin. As a result, icefishes display derived physiology that limits them to the cold and highly oxygenated Antarctic waters. Against these constraints, remarkably one species, the pike icefish Champsocephalus esox, successfully colonized temperate South American waters. To study the genetic mechanisms underlying secondarily temperate adaptation in icefishes, we generated chromosome-level genome assemblies of both C. esox and its Antarctic sister species, Champsocephalus gunnari. The C. esox genome is similar in structure and organization to that of its Antarctic congener; however, we observe evidence of chromosomal rearrangements coinciding with regions of elevated genetic divergence in pike icefish populations. We also find several key biological pathways under selection, including genes related to mitochondria and vision, highlighting candidates behind temperate adaptation in C. esox. Substantial antifreeze glycoprotein (AFGP) pseudogenization has occurred in the pike icefish, likely due to relaxed selection following ancestral escape from Antarctica. The canonical AFGP locus organization is conserved in C. esox and C. gunnari, but both show a translocation of two AFGP copies to a separate locus, previously unobserved in cryonotothenioids. Altogether, the study of this secondarily temperate species provides an insight into the mechanisms underlying adaptation to ecologically disparate environments in this otherwise highly specialized group.     

ANTAGONISTIC PLEIOTROPIC EFFECT OF SECOND-CHROMOSOME INVERSIONS ON BODY SIZE AND EARLY LIFE-HISTORY TRAITS IN DROSOPHILA BUZZATII

A simple way to think of evolutionary trade-offs is to suppose genetic effects of opposed direction that give rise to antagonistic pleiotropy. Maintenance of additive genetic variability for fitness related characters, in association with negative correlations between these characters, may result. In the cactophilic species Drosophila buzzatii, there is evidence that second-chromosome polymorphic inversions affect size-related traits. Because a trade-off between body size and larval developmental time has been reported in Drosophila, we study here whether or not these inversions also affect larva-adult viability and developmental time. In particular, we expect that polymorphic inversions make a statistically significant contribution to the genetic correlation between body size (as measured by thorax length) and larval developmental time. This contribution is expected to be in the direction predicted by the trade-off, namely, those flies whose karyotypes cause them to be genetically larger should also have a longer developmental time than flies with other karyotypes. Using two different experimental approaches, a statistically significant contribution of the second-chromosome inversions to the phenotypic variances of body size and developmental time in D. buzzatii was found. Further, these inversions make a positive contribution to the total genetic correlation between the traits, as expected by the suggested trade-off. The data do not provide evidence as to whether the genetic correlation is due to antagonistic pleiotropic gene action or to gametic disequilibrium of linked genes that affect one or both traits. The results do suggest, however, a possible explanation for the maintenance of inversion polymorphism in this species.     

A test of the chromosomal rearrangement model of speciation in Drosophila pseudoobscura

Recent studies suggest that chromosomal rearrangements play a significant role in speciation by preventing recombination and maintaining species persistence despite interspecies gene flow. Factors conferring adaptation or reproductive isolation are maintained in rearranged regions in the face of hybridization, while such factors are eliminated from collinear regions. As a direct test of this rearrangement model, we evaluated the genetic basis of hybrid male sterility in a sympatric species pair, Drosophila pseudoobscura pseudoobscura and D. persimilis, and an allopatric species pair, D. pseudoobscura bogotana and D. persimilis. Our results are consistent with the proposed model: virtually all of the sterility factors in the former pair are associated with three inverted regions, whereas sterility factors are present in the collinear regions in the latter pair. These findings indicate recombination and selection may have eliminated sterility factors outside the inverted regions between D. p. pseudoobscura and D. persimilis, suggesting chromosomal rearrangements may facilitate species persistence despite hybridization.     

On the Structural Plasticity of the Human Genome: Chromosomal Inversions Revisited

With the aid of novel and powerful molecular biology techniques, recent years have witnessed a dramatic increase in the number of studies reporting the involvement of complex structural variants in several genomic disorders. In fact, with the discovery of Copy Number Variants (CNVs) and other forms of unbalanced structural variation, much attention has been directed to the detection and characterization of such rearrangements, as well as the identification of the mechanisms involved in their formation. However, it has long been appreciated that chromosomes can undergo other forms of structural changes - balanced rearrangements - that do not involve quantitative variation of genetic material. Indeed, a particular subtype of balanced rearrangement – inversions – was recently found to be far more common than had been predicted from traditional cytogenetics. Chromosomal inversions alter the orientation of a specific genomic sequence and, unless involving breaks in coding or regulatory regions (and, disregarding complex trans effects, in their close vicinity), appear to be phenotypically silent. Such a surprising finding, which is difficult to reconcile with the classical interpretation of inversions as a mechanism causing subfertility (and ultimately reproductive isolation), motivated a new series of theoretical and empirical studies dedicated to understand their role in human genome evolution and to explore their possible association to complex genetic disorders. With this review, we attempt to describe the latest methodological improvements to inversions detection at a genome wide level, while exploring some of the possible implications of inversion rearrangements on the evolution of the human genome.     

A combination of sexual and ecological divergence contributes to rearrangement spread during initial stages of speciation

Chromosomal rearrangements between sympatric species often contain multiple loci contributing to assortative mating, local adaptation and hybrid sterility. When and how these associations arise during the process of speciation remains a subject of debate. Here, we address the relative roles of local adaptation and assortative mating on the dynamics of rearrangement evolution by studying how a rearrangement covaries with sexual and ecological trait divergence within a species. Previously, a chromosomal rearrangement that suppresses recombination on the Z (sex) chromosome was identified in European corn borer moths (Ostrinia nubilalis). We further characterize this recombination suppressor and explore its association with variation in sex pheromone communication and seasonal ecological adaptation in pairs of populations that are divergent in one or both of these characteristics. Direct estimates of recombination suppression in pedigree mapping families indicated that more than 39% of the Z chromosome (encompassing up to ~10 megabases and ~300 genes) resides within a nonrecombining unit, including pheromone olfactory receptor genes and a major quantitative trait locus that contributes to ecotype differences (Pdd). Combining direct and indirect estimates of recombination suppression, we found that the rearrangement was occasionally present between sexually isolated strains (E vs. Z) and between divergent ecotypes (univoltine vs. bivoltine). However, it was only consistently present when populations differed in both sexual and ecological traits. Our results suggest that independent of the forces that drove the initial establishment of the rearrangement, a combination of sexual and ecological divergence is required for rearrangement spread during speciation.     

The DAIBAM MITE element is involved in the origin of one fixed and two polymorphic Drosophila virilis phylad inversions

Chromosomal inversions can originate from breakage and repair by non-homologous end-joining. Nevertheless, they can also originate from ectopic recombination between transposable elements located on the same chromosome inserted in opposite orientations. Here, we show that a MITE element (DAIBAM), previously involved in the origin of one Drosophila americana polymorphic inversion, is also involved in the origin of one fixed inversion between D. virilis and D. americana and another D. americana polymorphic inversion. Therefore, DAIBAM is responsible for at least 20% of the chromosomal rearrangements that are observed within and between species of the virilis phylad (D. virilis, D. lummei, D. novamexicana and D. americana), having thus played a significant role in the chromosomal evolution of this group of closely related species.     

Karyotypic changes associated to the dispersive potential on Pomacentridae (Pisces, Perciformes)

When comparing karyotypic diversification between freshwater and marine fish, a notable increase in modifications associated to the former environment can be noticed in relation to the latter one. This fact is related to the great number of physical partitions (barriers) that exist in continental waters. Furthermore, in the marine environment, the barriers to the gene flow are complex and not always identifiable, especially when considering the participation of dynamic factors such as currents and winds associated to the dispersive potentialities of a living group. Within Perciformes fish, the Pomacentridae family stands out from the others for its intimate relation with the coral reefs, as well as for its diversity of forms and biological characteristics, providing an adequate model for studying the influence of the pelagic period of the larval stage upon the karyotypic evolution. In the present work, cytogenetic analyses were carried out on three Pomacentridae species, typical representatives of the coral reefs, Abudefduf saxatilis (2n=48, FN=52, 2 m+2sm+44a), Microspathodon chrysurus (2n=48, FN=64, 6 m+10st+32a) and Amphiprion frenatus (2n=48, FN=92, 14 m+22sm+8st+4a) that have different pelagic larval periods. The analyses between subfamilies showed a trend that the lower the dispersive potential, the greater the quantity of fixed pericentric inversions based on the basal karyotype of the Perciformes.     

Genetic Basis of a Violation of Dollo’s Law: Re-Evolution of Rotating Sex Combs in Drosophila bipectinata

Phylogenetic analyses suggest that violations of “Dollo’s law”—that is, re-evolution of lost complex structures—do occur, albeit infrequently. However, the genetic basis of such reversals has not been examined. Here, we address this question using the Drosophila sex comb, a recently evolved, male-specific morphological structure composed of modified bristles. In some species, sex comb development involves only the modification of individual bristles, while other species have more complex “rotated” sex combs that are shaped by coordinated migration of epithelial tissues. Rotated sex combs were lost in the ananassae species subgroup and subsequently re-evolved, ∼12 million years later, in Drosophila bipectinata and its sibling species. We examine the genetic basis of the differences in sex comb morphology between D. bipectinata and D. malerkotliana, a closely related species with a much simpler sex comb representing the ancestral condition. QTL mapping reveals that >50% of this difference is controlled by one chromosomal inversion that covers ∼5% of the genome. Several other, larger inversions do not contribute appreciably to the phenotype. This genetic architecture suggests that rotating sex combs may have re-evolved through changes in relatively few genes. We discuss potential developmental mechanisms that may allow lost complex structures to be regained.     

There large inversions in the chloroplast genomes and one loss of the chloroplast generps16 suggest an early evolutionary split in the genusAdonis (Ranunculaceae)

Detailed chloroplast DNA restriction site maps for two species in the genusAdonis (Ranunculaceae),A. annua andA. vernalis, were constructed using single and double digests and the sizes of these genomes are 151.3 and 156.5 kilobases, respectively. Three inversions were found inAdonis, relative to the gene order in the majority of land plants. These rearrangements represent two different gene orders and mark an ancient split in the evolutionary history of this genus. Gene probes were used in order to map the endpoints of the inversions and the inverted repeat regions. The inverted repeat is approximately 400 base pairs shorter inA. annua than inA. vernalis. Two inversions, 39 kilobases and 24 kilobases in size, occur inA. annua and one inversion, 42 kilobases in size, is present in the remaining investigated species ofAdonis. The generps16 is absent from the chloroplast genome inAdonis annua. Restriction sites for eleven restriction endonucleases were mapped forA. annua, A. vernalis and four additional species ofAdonis and two species ofTrollius. Eighty-six phylogenetically informative sites were analysed cladistically in order to evaluate the main clades withinAdonis.