Selection on quantitative traits by divergent climatic conditions can lead to substantial trait variation across a species range. In the context of rapidly changing environments, however, it is equally important to understand selection on trait plasticity. To evaluate the role of selection in driving divergences in traits and their associated plasticity within a widespread species, we compared molecular and quantitative trait variation in Populus fremontii (Fremont cottonwood) populations throughout Arizona. Using SNP data and genotypes from 16 populations reciprocally planted in three common gardens, we first performed QST-FST analyses to detect selection on traits and trait plasticity. We then explored the mechanistic basis of selection using trait-climate and plasticity-climate regressions. Three major findings emerged: 1) There was significant genetic variation in traits expressed in each of the common gardens and in the phenotypic plasticity of traits across gardens. 2) Based on QST-FST comparisons, there was evidence of selection in all traits measured; however, this result varied from no effect in one garden to highly significant in another, indicating that detection of past selection is environmentally dependent. We also found strong evidence of divergent selection on plasticity across environments for two traits. 3) Traits and/or their plasticity were often correlated with population source climate (R2 up to 0.77 and 0.66, respectively). This suggests that steep climate gradients across the Southwest have played a major role in shaping the evolution of divergent phenotypic responses in populations and genotypes now experiencing climate change.
Growing genetically resistant plants allows pathogen populations to be controlled and reduces the use of chemicals. However, pathogens can quickly overcome such resistance. In this context, how can we achieve sustainable crop protection? This crucial question has remained largely unanswered despite decades of intense debate and research effort. In this study, we used a bibliographic analysis to show that the research field of resistance durability has evolved into three subfields: (i) ‘plant breeding’ (generating new genetic material), (ii) ‘molecular interactions’ (exploring the molecular dialogue governing plant–pathogen interactions) and (iii) ‘epidemiology and evolution’ (explaining and forecasting of pathogen population dynamics resulting from selection pressure(s) exerted by resistant plants). We argue that this triple split of the field impedes integrated research progress and ultimately compromises the sustainable management of genetic resistance. After identifying a gap among the three subfields, we argue that the theoretical framework of population genetics could bridge this gap. Indeed, population genetics formally explains the evolution of all heritable traits, and allows genetic changes to be tracked along with variation in population dynamics. This provides an integrated view of pathogen adaptation, notably via evolutionary–epidemiological feedbacks. In this Opinion Note, we detail examples illustrating how such a framework can better inform best practice for developing and managing genetically resistant cultivars.
Invasive species are among the most important, growing threats to food security and agricultural systems. The Mediterranean fruit fly Ceratitis capitata is one of the most damaging representatives of a group of rapidly expanding species in the family Tephritidae due to their wide host range and high invasiveness. Here, we used restriction site-associated DNA sequencing (RADseq) to investigate population genomic structure and phylogeographic history of medflies collected from six sampling sites, including Africa (South Africa), the Mediterranean (Spain, Greece), Latin America (Guatemala, Brazil) and Australia. A total of 1,907 single nucleotide polymorphisms (SNPs) showed two genetic clusters separating native and introduced ranges, consistent with previous findings. In the introduced range, all individuals were assigned to one genetic cluster except for those in Brazil, which showed introgression of a genetic cluster that also appeared exclusively in South Africa and could not be previously identified using microsatellite markers. Moreover, the microbiome variations in medfly populations from selected sampling sites was assessed by amplicon sequencing of the 16S ribosomal RNA (V4 region). No strong patterns of microbiome variation were detected across geographic regions or host plants, except for the differentiation of the Brazilian specimens which showed increased diversity and unique composition of its microbiome compared to other sampling sites. The unique SNP patterns in the Brazilian specimens could point to a direct migration route from Africa with subsequent adaptation of the microbiota to the specific conditions present in Brazil. These findings significantly improve our understanding of the evolutionary history of global medfly invasions and adaptation to newly colonised environments.
Inducible defenses of prey are evolved under diverse and variable predation risks. However, during the co-evolution of prey and multiple predators, the responses of prey to antagonistic predation risks, which may put the prey into a dilemma of responding to predators, remain unclear. Based on antagonistic predation pressure from an invertebrate (Chaoborus larvae) and a vertebrate (Rhodeus ocellatus) predator, we studied the responses of multiple traits and transcriptomes of the freshwater crustacean Ceriodaphnia cornuta under multiple predation risks. Chaoborus predation risk altered the expression of genes encoding cuticle proteins and modulated the biosynthesis of steroid hormones, cutin, suberine, and wax, leading to the development of horns and increase in size at the late developmental stage. Meanwhile, fish predation risk primarily triggered genes encoding ribosomes and those involved in unsaturated fatty acid biosynthesis and cysteine and methionine metabolism, resulting in smaller individual size and earlier reproduction. Inducible responses of both transcriptome and individual traits revealed that predator-dependent unique responses were dominant and the dilemma of antagonistic responses was relatively limited. However, the unique individual traits in response to invertebrate predation could be significantly impaired by vertebrate predation risk, even though the unique responses to different predators were extremely weakly correlated and could be elicited simultaneously. These results indicate that diverse predator-dependent unique responses are favored by Ceriodaphnia during its co-evolution with multiple predators. Nonetheless, Ceriodaphnia is not a generalist that can fully adopt all predator-dependent unique responses simultaneously under multiple predation risks.
Understanding ageing and the diversity of life histories is a cornerstone in biology. Telomeres, the protecting caps of chromosomes, are thought to be involved in ageing, cancer risks and to modulate life-history strategies. They shorten with cell division and age in somatic tissues of most species, possibly limiting lifespan. The resource allocation trade-off hypothesis predicts that short telomeres have thus co-evolved with early reproduction, proactive behaviour and reduced lifespan: a fast Pace-of-Life Syndrome (POLS). Conversely, since short telomeres may also reduce the risks of cancer, the anti-cancer hypothesis advances that they should be associated with slow POLS. Conclusion on which hypothesis best supports the role of telomeres as mediators of life-history strategies is hampered by a lack of study on wild short-lived vertebrates, apart from birds. Using seven years of data on wild Eastern chipmunks Tamias striatus, we highlighted that telomeres elongate with age and do not limit lifespan in this species. Furthermore, short telomeres correlated with a slow POLS in a sex-specific way. Females with short telomeres had a delayed age at first breeding and a lower fecundity rate than females with long telomeres, whereas those differences were not recorded in males. Our findings support most predictions adapted from the anti-cancer hypothesis, but none of those made under the resource allocation trade-off hypothesis. Results are in line with an increasing body of evidence suggesting that other evolutionary forces than resource allocation trade-offs shape the diversity of telomere length in adult somatic cells and the relationships between telomeres and life-histories.
Sympatric speciation was once thought most improbable, but careful study of some systems, particularly the apple maggot (Rhagoletis pomonella) and related Rhagoletis species has led to a re-evaluation of its likelihood. Different species and host races in this clade of flies often have highly specialized host preference, and along with frequent evolutionary shifts to different fruit species between sister taxa, there is a likely effect of the timing of adult emergence that follows host fruiting phenology. This is known as “allochronic” isolation (from the Greek, meaning “different timing”). This overview covers recent discoveries by Inskeep et al. (2021) showing how allochrony is a major factor in preventing gene flow between a pair of sister species of Rhagoletis on different host fruits. Although the authors do not claim to prove sympatric speciation, it does seem very likely, and the work clearly underscores how readily host shifts via allochrony can aid sympatric speciation.
Geographically connected species pairs with weakly differentiated genomes could either represent cases of genomic homogenization in progress or of incipient parapatric speciation. Discriminating between these processes is difficult because intermediate stages of either may produce weakly differentiated genomes that diverge at few locations. We used coalescent modelling applied to a genome-wide sample of SNPs to discriminate between speciation with gene flow and genomic homogenization in two phenotypically distinct but genomically weakly diverged species of elevationally replacing Ramphocelus tanagers, forming a hybrid zone in the Andean foothills. We found overwhelming support for a model of genomic homogenization following secondary contact. Simulating under this model suggested that our species pair was differentiated (FST = 0.30) at secondary contact but that most of the genome has rapidly homogenized during 254 Ky of high gene flow towards the present (FST = 0.02). Despite extensive genome-wide homogenization, plumage remains distinctive with a narrower than expected geographic cline width, indicating divergent selection on colour. We found two SNPs significantly associated with plumage colour, which retain moderately high FST. We conclude that the majority of the genome has fused, but that divergent selection on select loci probably maintains the geographically structured colour differences between these incipient species.
Understanding how populations diverge and new species arise is a central question in evolutionary biology. ‘Allopatric’ divergence through geographic isolation is considered to be the commonest mechanism generating species biodiversity in mountainous ecosystems. However, the underlying genomic dynamics, especially genomic islands of elevated divergence and genes that are highly diverged as a result of lineage-specific selection, remain poorly understood. Stellera chamaejasme is widely distributed on the Qinghai-Tibet Plateau and in adjacent regions, making it a good model with which to explore genomic divergence in mountainous ecosystems. We assembled a high-quality, chromosome-level genome for this species and re-sequenced the genomes of 24 populations across its distributional range. Our population genomic analyses recovered four distinct genetic lineages corresponding to geographic distributions with contrasting environments. However, we revealed that continuous gene flow occurred during the diversification of these four lineages and inter-lineage hybrids, and plastome introgressions were frequently found in regions of contact. The elevated genomic divergences were highly heterogeneous across the genome. The formation of such genomic islands showed neither correlation with rate of gene flow nor relationship to time of divergence. The lineage-specific positively selected genes potentially involved in local adaptation were found both within and outside genomic islands. Our results suggest that genomic divergence in S. chamaejasme is likely to have been triggered and further maintained by local selection in addition to geographic isolation.
Lineage-based species definitions applying coalescent approaches to species delimitation have become increasingly popular. Yet, the application of these methods and the recognition of lineage-only definitions have recently been questioned. Species delimitation criteria that explicitly consider both lineages and evidence for ecological ‘role’ shifts provide an opportunity to incorporate ecologically meaningful data from multiple sources in studies of species boundaries. Here, such criteria were applied to a problematic group of mycoheterotrophic orchids, the Corallorhiza striata complex, analyzing genomic, morphological, phenological, reproductive-mode, niche, and fungal host data. A recently developed method for generating genomic polymorphism data–ISSRseq–demonstrates evidence for four distinct lineages, including a previously unidentified lineage in the Coast Ranges and Cascades of California and Oregon, USA. There is divergence in morphology, phenology, reproductive mode, and fungal associates among the four lineages. Integrative analyses, conducted in population assignment and redundancy analysis frameworks, provide evidence of distinct genomic lineages and a similar pattern of divergence in the ‘extended’ data, albeit with weaker signal. However, none of the ‘extended’ datasets fully satisfy the condition of a significant ‘role’ shift, which requires evidence of fixed differences. The four lineages identified in the current study are recognized at the level of variety, short of comprising different species. This study represents the most comprehensive application of ‘lineage+role’ to date and illustrates the advantages of such an approach.
Host-specialist parasites of endangered large vertebrates are in many cases more endangered than their hosts. In particular, low population densities and reduced among-host transmission rates are expected to lead to inbreeding within parasite infrapopulations living on single host individuals. Furthermore, spatial population structures of directly-transmitted parasites should be concordant with those of their hosts. Using population genomic approaches, we investigated inbreeding and population structure in a host-specialist seal louse (Echinophthirius horridus) infesting the Saimaa ringed seal (Phoca hispida saimensis), which is endemic to Lake Saimaa in Finland, and is one of the most endangered pinnipeds in the world. We conducted genome resequencing of pairs of lice collected from 18 individual Saimaa ringed seals throughout the Lake Saimaa complex. Our analyses showed high genetic similarity and inbreeding between lice inhabiting the same individual seal host, indicating low among-host transmission rates. Across the lake, genetic differentiation among individual lice was correlated with their geographic distance, and assignment analyses revealed a marked break in the genetic variation of the lice in the middle of the lake, indicating substantial population structure. These findings indicate that movements of Saimaa ringed seals across the main breeding areas of the fragmented Lake Saimaa complex may in fact be more restricted than suggested by previous population-genetic analyses of the seals themselves.
By their paternal transmission, Y-chromosomal haplotypes are sensitive markers of population history and male-mediated introgression. Previous studies identified biallelic single-nucleotide variants in the SRY, ZFY, DDX3Y genes, which in domestic goats identified four major Y-chromosomal haplotypes Y1A, Y1B, Y2A and Y2B with a marked geographic partitioning. Here, we analyze whole-genome sequences of 386 domestic goats from 75 modern breeds and 7 wild goat species that were generated by the VarGoats goat genome project. Phylogenetic analyses indicated domestic haplogroups corresponding to Y1B, Y2A and Y2B, respectively, whereas Y1A is split into Y1AA and Y1AB. All five haplogroups were detected in 26 ancient DNA samples from southeast Europe or Asia. Haplotypes from present-day bezoars are not shared with domestic goats and are attached to deep nodes of the trees and networks. Haplogroup distributions for 180 domestic breeds indicate ancient paternal population bottlenecks and expansions during the migrations into northern Europe, eastern and southern Asia and Africa south of the Sahara. In addition, sharing of haplogroups indicates male-mediated introgressions, most notably an early gene flow from Asian goats into Madagascar and the crossbreeding that in the 19th century resulted in the popular Boer and Anglo-Nubian breeds. More recent introgressions are those from European goats into the native Korean goat population and from Boer goat into Uganda, Kenya, Tanzania, Malawi and Zimbabwe. This study illustrates the power of the Y-chromosomal variants for reconstructing the history of domestic species with a wide geographic range.
The role of methylation in adaptive, developmental and speciation processes has attracted considerable interest, but interpretation of results is complicated by diffuse boundaries between genetic and non-genetic variation. We studied whole genome genetic and methylation variation in the European eel, distributed from subarctic to subtropical environments, but with panmixia precluding genetically based local adaptation beyond single-generation responses. Overall methylation was 70.9%, with hypomethylation predominantly found in promoters and first exons. Redundancy analyses involving juvenile glass eels showed 0.06% and 0.03% of the variance at SNPs to be explained by localities and environmental variables, respectively, with GO terms of genes associated with outliers primarily involving neural system functioning. For CpGs 2.98% and 1.36% of variance was explained by localities and environmental variables. Differentially methylated regions particularly included genes involved in developmental processes, with hox clusters featuring prominently. Life stage (adult versus glass eels) was the most important source of inter-individual variation in methylation, likely reflecting both ageing and developmental processes. Demethylation of transposable elements was observed in European X American eel hybrids, possibly representing postzygotic barriers in this system characterized by prolonged speciation and ongoing gene flow. Whereas the genetic data are consistent with a role of single-generation selective responses, the methylation results underpin the importance of epigenetics in the life cycle of eels and suggests interactions between local environments, development and phenotypic variation mediated by methylation variation. Eels are remarkable by having retained eight hox clusters, and the results suggest important roles of methylation at hox genes for adaptive processes.
Gracilaria chilensis is the main cultivated seaweed in Chile. The low genetic diversity observed in the Chilean population has been associated with the over-exploitation of natural beds and/or the founder effect that occurred during the post-glacial colonization from New Zealand. How these processes have affected its evolutionary trajectory before farming and incipient domestication is poorly understood. In this study, we used 2,232 SNPs to assess how the species evolutionary history in New Zealand (its region of origin), the founder effect linked to transoceanic dispersion and colonization of South America, and the recent over-exploitation of natural populations have influenced the genetic architecture of G. chilensis in Chile. The contrasting patterns of genetic diversity and structure observed between the two main islands in New Zealand attest to the important effects of Quaternary glacial cycles on G. chilensis. ABC analyses indicated that Chatham Island and South America were colonized independently near the end of the Last Glacial Maximum and emphasized the importance of coastal and oceanic currents during that period. Furthermore, ABC analyses inferred the existence of a recent and strong genetic bottleneck in Chile, matching the period of over-exploitation of the natural beds during the 1970s, followed by rapid demographic expansion linked to active clonal propagation used in farming. Recurrent genetic bottlenecks strongly eroded the genetic diversity of G. chilensis prior to its cultivation, raising important challenges for the management of genetic resources in this incipiently domesticated species.
Natural hybrid zones provide opportunities for studies of the evolution of reproductive isolation in wild populations. Although recent investigations have found that the formation of neo-sex chromosomes is associated with reproductive isolation, the mechanisms remain unclear in most cases. Here, we assess the contemporary structure of gene flow in the contact zone between largely allopatric cytotypes of the dioecious plant Rumex hastatulus, a species with evidence of sex chromosome turn-over. Males to the west of the Mississippi river, USA, have an X and a single Y chromosome, whereas populations to the east of the river have undergone a chromosomal rearrangement giving rise to a larger X and two Y chromosomes. Using reduced-representation sequencing, we provide evidence that hybrids form readily and survive multiple backcross generations in the field, demonstrating the potential for ongoing gene flow between the cytotypes. Cline analysis of each chromosome separately captured no signals of difference in cline shape between chromosomes. However, principal component regression revealed a significant increase in the contribution of individual SNPs to inter-cytotype differentiation on the neo-X chromosome, but no correlation with recombination rate. Cline analysis revealed that the only SNPs with significantly shallower clines than the genome-average were located on the neo-X. Our data are consistent with a role for neo-sex chromosomes in reproductive isolation between R. hastatulus cytotypes. Our investigation highlights the importance of studying plant hybrid zones in species with sex chromosomes for understanding mechanisms of reproductive isolation and the role of gene flow in the spread of neo-X chromosomes.
Insecticide resistance provides both a pressing threat to the control of vector-borne diseases and insights into the remarkable capacity of natural populations to show rapid evolutionary responses. Malaria control remains heavily dependent on deployment of insecticides, primarily in long lasting insecticide treated nets (LLINs), but resistance in the major malaria vectors has increased over the last 15 years. Identifying genetic mechanisms causing high-level resistance in mosquitoes, which may almost entirely overcome pyrethroid efficacy, is crucial for the development and deployment of potentially resistance-breaking tools. Using the Anopheles gambiae 1000 genomes data we identified a very recent selective sweep in Ugandan mosquitoes which localized to a cluster of cytochrome P450 genes. Further interrogation revealed a haplotype involving a trio of mutations, a point mutation in Cyp6p4, an insertion of a partial Zanzibar transposable element (TE) and a duplication of the Cyp6aa1 gene. The mutations appear to have originated recently in An. gambiae from the Kenya-Uganda border region, with stepwise replacement of the double-mutant (Zanzibar TE and Cyp6p4-236M) with the triple-mutant haplotype (including Cyp6aa1 duplication), which has spread into the Democratic Republic of Congo and Tanzania. The triple-mutant haplotype is strongly associated with increased expression of genes able to metabolise pyrethroids; is strongly predictive of resistance to pyrethroids but importantly, appears less effective against LLINs co-treated with the synergist piperonyl butoxide (PBO). Frequencies of the triple-mutant haplotype remain spatially variable even within countries, suggesting an effective marker system to guide deployment decisions for limited supplies of PBO-pyrethroid co-treated LLINs across African countries.
Synteny, the ordering of sequences within homologous chromosomes, must be maintained within the genomes of sexually reproducing species for the sharing of alleles and production of viable, reproducing offspring. However, when the genomes of closely related species are compared, a loss of synteny can be observed. Synteny loss may be occurring due to transposon-mediated recombination errors during meiosis, unequal homologous recombination, resulting in the formation of chromosomal rearrangements. To examine patterns of synteny amongst three closely related, interbreeding, and wild Eucalyptus species, we assembled their genomes using long-read DNA sequencing and de novo assembly. We identify syntenic and rearranged regions between these genomes and estimate that ~48% of our genomes remain syntenic while ~36% is rearranged. We observed that rearrangements highly fragment micro-synteny, however genome-wide, macro-synteny appears to be maintained. Our results suggest that synteny between our species is primarily lost through small-scale rearrangements, not through sequence loss, gain, or sequence divergence. Further examination of identified rearrangements suggests that rearrangements may be altering the phenotypes of Eucalyptus species. Our study also questions the use of single reference genomes in genomic studies, reliance on a single reference genome when seeking genetic variation leads to reference bias, especially given the scale at which we show potentially adaptive loci have highly diverged, deleted, duplicated and/or rearranged. This study provides an unbiased framework to look at potential speciation and adaptive loci among a rapidly radiating foundation species of woodland trees that are free from selective breeding seen in most crop species.
Disseminated neoplasia (DN) is one of the most challenging and unrecognised diseases occurring in aquatic fauna. It has been diagnosed in four bivalve species from the Gulf of Gdańsk (Southern Baltic Sea) with the highest frequency in Limecola balthica (formerly Macoma balthica), reaching up to 94% in some populations. The aetiology of DN in the Baltic Sea has not yet been identified, with earlier studies trying to link its occurrence with environmental pollution. Taking into account recent research providing evidence that DN is horizontally transmitted as clonal cells between individuals in some bivalve species, we aimed to test whether DN is a transmissible cancer in the population of L. balthica from the Gulf of Gdańsk highly affected with cancer. We examined mitochondrial cytochrome c oxidase I (mtCOI) and elongation factor 1α (EF1α) sequences of genomes obtained from haemolymph and tissues of neoplastic and healthy individuals. Sequence analysis resulted in detection of an independent transmissible cancer lineage occurring in 4 neoplastic clams that is not present in healthy animals. This paper describes the first case of transmissible DN in the clam L. balthica providing further insights for studies on this disease.
We recently published a paper quantifying the genome-wide consequences of natural selection, including the effects of indirect selection due to the correlation of genetic regions (neutral or selected) with directly selected regions (Gompert et al. 2022). In their critique of our paper, Charlesworth & Jensen (2022) make two main points: (i) indirect selection is equivalent to hitchhiking and thus well documented (i.e., our results are not novel), and (ii) that we do not demonstrate the source of linkage disequilibrium (LD) between SNPs and the Mel-Stripe locus in the Timema cristinae experiment we analyze. As we discuss in detail below, neither of these are substantial criticisms of our work.