Genomically correlated trait combinations and antagonistic selection contributing to counterintuitive genetic patterns of adaptive diapause divergence in Rhagoletis flies.

Adaptation to novel environments can result in unanticipated genomic responses to selection. Here, we illustrate how multifarious, correlational selection helps explain a counterintuitive pattern of genetic divergence between the recently derived apple- and ancestral hawthorn-infesting host races of Rhagoletis pomonella (Diptera: Tephritidae). The apple host race terminates diapause and emerges as adults earlier in the season than the hawthorn host race, to coincide with the earlier fruiting phenology of their apple hosts. However, alleles at many loci associated with later emergence paradoxically occur at higher frequencies in sympatric populations of the apple compared to the hawthorn race. We present genomic evidence that historical selection over geographically varying environmental gradients across North America generated genetic correlations between two life history traits, diapause intensity and diapause termination, in the hawthorn host race. Moreover, the loci associated with these life history traits are concentrated in genomic regions in high linkage disequilibrium (LD). These genetic correlations are antagonistic to contemporary selection on local apple host race populations that favours increased initial diapause depth and earlier, not later, diapause termination. Thus, the paradox of apple flies appears due, in part, to pleiotropy or linkage of alleles associated with later adult emergence and increased initial diapause intensity, the latter trait strongly selected for by the earlier phenology of apples. Our results demonstrate how understanding of multivariate trait combinations and the correlative nature of selective forces acting on them can improve predictions concerning adaptive evolution and help explain seemingly counterintuitive patterns of genetic diversity in nature.

Testing the potential contribution of Wolbachia to speciation when cytoplasmic incompatibility becomes associated with host-related reproductive isolation.

Endosymbiont-induced cytoplasmic incompatibility (CI) may play an important role in arthropod speciation. However, whether CI consistently becomes associated or coupled with other host-related forms of reproductive isolation (RI) to impede the transfer of endosymbionts between hybridizing populations and further the divergence process remains an open question. Here, we show that varying degrees of pre- and postmating RI exist among allopatric populations of two interbreeding cherry-infesting tephritid fruit flies (Rhagoletis cingulata and R. indifferens) across North America. These flies display allochronic and sexual isolation among populations, as well as unidirectional reductions in egg hatch in hybrid crosses involving southwestern USA males. All populations are infected by a Wolbachia strain, wCin2, whereas a second strain, wCin3, only co-infects flies from the southwest USA and Mexico. Strain wCin3 is associated with a unique mitochondrial DNA haplotype and unidirectional postmating RI, implicating the strain as the cause of CI. When coupled with nonendosymbiont RI barriers, we estimate the strength of CI associated with wCin3 would not prevent the strain from introgressing from infected southwestern to uninfected populations elsewhere in the USA if populations were to come into secondary contact and hybridize. In contrast, cytoplasmic-nuclear coupling may impede the transfer of wCin3 if Mexican and USA populations were to come into contact. We discuss our results in the context of the general paucity of examples demonstrating stable Wolbachia hybrid zones and whether the spread of Wolbachia among taxa can be constrained in natural hybrid zones long enough for the endosymbiont to participate in speciation.

Evidence for spatial clines and mixed geographic modes of speciation for North American cherry-infesting Rhagoletis (Diptera: Tephritidae) flies.

An important criterion for understanding speciation is the geographic context of population divergence. Three major modes of allopatric, parapatric, and sympatric speciation define the extent of spatial overlap and gene flow between diverging populations. However, mixed modes of speciation are also possible, whereby populations experience periods of allopatry, parapatry, and/or sympatry at different times as they diverge. Here, we report clinal patterns of variation for 21 nuclear-encoded microsatellites and a wing spot phenotype for cherry-infesting Rhagoletis (Diptera: Tephritidae) across North America consistent with these flies having initially diverged in parapatry followed by a period of allopatric differentiation in the early Holocene. However, mitochondrial DNA (mtDNA) displays a different pattern; cherry flies at the ends of the clines in the eastern USA and Pacific Northwest share identical haplotypes, while centrally located populations in the southwestern USA and Mexico possess a different haplotype. We hypothesize that the mitochondrial difference could be due to lineage sorting but more likely reflects a selective sweep of a favorable mtDNA variant or the spread of an endosymbiont. The estimated divergence time for mtDNA suggests possible past allopatry, secondary contact, and subsequent isolation between USA and Mexican fly populations initiated before the Wisconsin glaciation. Thus, the current genetics of cherry flies may involve different mixed modes of divergence occurring in different portions of the fly's range. We discuss the need for additional DNA sequencing and quantification of prezygotic and postzygotic reproductive isolation to verify the multiple mixed-mode hypothesis for cherry flies and draw parallels from other systems to assess the generality that speciation may commonly involve complex biogeographies of varying combinations of allopatric, parapatric, and sympatric divergence.

Geographic and Ecological Dimensions of Host Plant-Associated Genetic Differentiation and Speciation in the Rhagoletis cingulata (Diptera: Tephritidae) Sibling Species Group.

Ascertaining the causes of adaptive radiation is central to understanding how new species arise and come to vary with their resources. The ecological theory posits adaptive radiation via divergent natural selection associated with novel resource use; an alternative suggests character displacement following speciation in allopatry and then secondary contact of reproductively isolated but ecologically similar species. Discriminating between hypotheses, therefore, requires the establishment of a key role for ecological diversification in initiating speciation versus a secondary role in facilitating co-existence. Here, we characterize patterns of genetic variation and postzygotic reproductive isolation for tephritid fruit flies in the Rhagoletis cingulata sibling species group to assess the significance of ecology, geography, and non-adaptive processes for their divergence. Our results support the ecological theory: no evidence for intrinsic postzygotic reproductive isolation was found between two populations of allopatric species, while nuclear-encoded microsatellites implied strong ecologically based reproductive isolation among sympatric species infesting different host plants. Analysis of mitochondrial DNA suggested, however, that cytoplasmic-related reproductive isolation may also exist between two geographically isolated populations within R cingulata. Thus, ecology associated with sympatric host shifts and cytoplasmic effects possibly associated with an endosymbiont may be the key initial drivers of the radiation of the R. cingulata group.

Genomic Differentiation during Speciation-with-Gene-Flow: Comparing Geographic and Host-Related Variation in Divergent Life History Adaptation in Rhagoletis pomonella.

A major goal of evolutionary biology is to understand how variation within populations gets partitioned into differences between reproductively isolated species. Here, we examine the degree to which diapause life history timing, a critical adaptation promoting population divergence, explains geographic and host-related genetic variation in ancestral hawthorn and recently derived apple-infesting races of Rhagoletis pomonella. Our strategy involved combining experiments on two different aspects of diapause (initial diapause intensity and adult eclosion time) with a geographic survey of genomic variation across four sites where apple and hawthorn flies co-occur from north to south in the Midwestern USA. The results demonstrated that the majority of the genome showing significant geographic and host-related variation can be accounted for by initial diapause intensity and eclosion time. Local genomic differences between sympatric apple and hawthorn flies were subsumed within broader geographic clines; allele frequency differences within the races across the Midwest were two to three-fold greater than those between the races in sympatry. As a result, sympatric apple and hawthorn populations displayed more limited genomic clustering compared to geographic populations within the races. The findings suggest that with reduced gene flow and increased selection on diapause equivalent to that seen between geographic sites, the host races may be recognized as different genotypic entities in sympatry, and perhaps species, a hypothesis requiring future genomic analysis of related sibling species to R. pomonella to test. Our findings concerning the way selection and geography interplay could be of broad significance for many cases of earlier stages of divergence-with-gene flow, including (1) where only modest increases in geographic isolation and the strength of selection may greatly impact genetic coupling and (2) the dynamics of how spatial and temporal standing variation is extracted by selection to generate differences between new and discrete units of biodiversity.

High-pressure effect on the dynamics of solvated peptides.

The dynamics of peptides has a direct connection to how quickly proteins can alter their conformations. The speed of exploring the free energy landscape depend on many factors, including the physical parameters of the environment, such as pressure and temperature. We performed a series of molecular dynamics simulations to investigate the pressure-temperature effects on peptide dynamics, especially on the torsional angle and peptide-water hydrogen bonding (H-bonding) dynamics. Here, we show that the dynamics of the omega angle and the H-bonding dynamics between water and the peptide are affected by pressure. At high temperature (500 K), both the dynamics of the torsional angle ω and H-bonding slow down significantly with increasing pressure, interestingly, at approximately the same rate. However, at a lower temperature of 300 K, the observed trend on H-bonding dynamics as a function of pressure reverses, i.e., higher pressure speeds up H-bonding dynamics.

Stability and sugar recognition ability of ricin-like carbohydrate binding domains.

Lectins are a class of proteins known for their novel binding to saccharides. Understanding this sugar recognition process can be crucial in creating structure-based designs of proteins with various biological roles. We focus on the sugar binding of a particular lectin, ricin, which has two ß-trefoil carbohydrate-binding domains (CRDs) found in several plant protein toxins. The binding ability of possible sites of ricin-like CRD has been puzzling. The apo and various (multiple) ligand-bound forms of the sugar-binding domains of ricin were studied by molecular dynamics simulations. By evaluating structural stability, hydrogen bond dynamics, flexibility, and binding energy, we obtained a detailed picture of the sugar recognition of the ricin-like CRD. Unlike what was previously believed, we found that the binding abilities of the two known sites are not independent of each other. The binding ability of one site is positively affected by the other site. While the mean positions of different binding scenarios are not altered significantly, the flexibility of the binding pockets visibly decreases upon multiple ligand binding. This change in flexibility seems to be the origin of the binding cooperativity. All the hydrogen bonds that are strong in the monoligand state are also strong in the double-ligand complex, although the stability is much higher in the latter form due to cooperativity. These strong hydrogen bonds in a monoligand state are deemed to be the essential hydrogen bonds. Furthermore, by examining the structural correlation matrix, the two domains are structurally one entity. Galactose hydroxyl groups, OH4 and OH3, are the most critical parts in both site 1α and site 2γ recognition.