Source Of Evolutionary Novelty Research Articles

Pleistocene-dated genomic divergence of avocado trees supports cryptic diversity in the Colombian germplasm

Genomic characterization of ex situ plant collections optimizes the utilization of genetic resources by identifying redundancies among accessions, capturing cryptic variation, establishing reference collections, and ultimately assisting pre-breeding and breeding efforts. Yet, the integration of evolutionary genomic analyses is often lacking when studying the biodiversity of crop gene pools. Such is the case in the avocado, Persea americana Mill., an iconic American fruit tree crop that has seen an unprecedented expansion worldwide because of its nutritional properties. However, given a very restricted number of commercial clones, avocado plantations are becoming more vulnerable to diseases and climate change. Therefore, exploring new sources of evolutionary novelty and genetic diversity beyond the commercial varieties derived from traditional genetic pools in Mexico and Central America is imperative. To fill this gap, we aimed to characterize the genomic diversity of Colombian avocado trees. Specifically, we constructed reduced representation genomic libraries to genotype by sequencing 144 accessions from the Colombian National genebank and 240 materials from local commercial orchards in the Colombian northwest Andes. We merged the resulting reads with available sequences of reference genotypes from known avocado groups (also named as races), Mexican, Guatemalan, and West Indian, to discover 4931 SNPs. We then analyzed the population structure and phylogenetic diversity, and reconstructed evolutionary scenarios, possibly leading to new genetic groups in Colombian germplasm. We detected demographic stratification despite evidence of intergroup gene flow. Besides the classical three avocado groups, we found an exclusive Colombian group with a possible genetic substructure related to the geographical origin (Andean and Caribbean). Phylogenetic and ABC demographic modeling suggested that the Colombian group evolved in the Pleistocene before human agriculture started, and its closest relative from the three recognized races would be the West Indian group. We conclude that northwest South America offers a cryptic source of allelic novelty capable of boosting avocado pre-breeding strategies to select rootstock candidates well adapted to specific eco-geographical regions in Colombia and abroad.

Environment-dependent epistasis increases phenotypic diversity in gene regulatory networks.

Mutations to gene regulatory networks can be maladaptive or a source of evolutionary novelty. Epistasis confounds our understanding of how mutations affect the expression patterns of gene regulatory networks, a challenge exacerbated by the dependence of epistasis on the environment. We used the toolkit of synthetic biology to systematically assay the effects of pairwise and triplet combinations of mutant genotypes on the expression pattern of a gene regulatory network expressed in Escherichia coli that interprets an inducer gradient across a spatial domain. We uncovered a preponderance of epistasis that can switch in magnitude and sign across the inducer gradient to produce a greater diversity of expression pattern phenotypes than would be possible in the absence of such environment-dependent epistasis. We discuss our findings in the context of the evolution of hybrid incompatibilities and evolutionary novelties.

DNA methylation signatures of duplicate gene evolution in angiosperms.

Gene duplication is a source of evolutionary novelty. DNA methylation may play a role in the evolution of duplicate genes (paralogs) through its association with gene expression. While this relationship has been examined to varying extents in a few individual species, the generalizability of these results at either a broad phylogenetic scale with species of differing duplication histories or across a population remains unknown. We applied a comparative epigenomics approach to 43 angiosperm species across the phylogeny and a population of 928 Arabidopsis (Arabidopsis thaliana) accessions, examining the association of DNA methylation with paralog evolution. Genic DNA methylation was differentially associated with duplication type, the age of duplication, sequence evolution, and gene expression. Whole genome duplicates were typically enriched for CG-only gene-body methylated or unmethylated genes, while single-gene duplications were typically enriched for non-CG methylated or unmethylated genes. Non-CG methylation, in particular, was characteristic of more recent single-gene duplicates. Core angiosperm gene families differentiated into those which preferentially retain paralogs and 'duplication-resistant' families, which convergently reverted to singletons following duplication. Duplication-resistant families that still have paralogous copies were, uncharacteristically for core angiosperm genes, enriched for non-CG methylation. Non-CG methylated paralogs had higher rates of sequence evolution, higher frequency of presence-absence variation, and more limited expression. This suggests that silencing by non-CG methylation may be important to maintaining dosage following duplication and be a precursor to fractionation. Our results indicate that genic methylation marks differing evolutionary trajectories and fates between paralogous genes and have a role in maintaining dosage following duplication.

Genetic architecture facilitates then constrains adaptation in a host–parasite coevolutionary arms race

In coevolutionary arms races, interacting species impose selection on each other, generating reciprocal adaptations and counter adaptations. This process is typically enhanced by genetic recombination and heterozygosity, but these sources of evolutionary novelty may be secondarily lost when uniparental inheritance evolves to ensure the integrity of sex-linked adaptations. We demonstrate that host-specific egg mimicry in the African cuckoo finch Anomalospiza imberbis is maternally inherited, confirming the validity of an almost century-old hypothesis. We further show that maternal inheritance not only underpins the mimicry of different host species but also additional mimetic diversification that approximates the range of polymorphic egg “signatures” that have evolved within host species as an escalated defense against parasitism. Thus, maternal inheritance has enabled the evolution and maintenance of nested levels of mimetic specialization in a single parasitic species. However, maternal inheritance and the lack of sexual recombination likely disadvantage cuckoo finches by stifling further adaptation in the ongoing arms races with their individual hosts, which we show have retained biparental inheritance of egg phenotypes. The inability to generate novel genetic combinations likely prevents cuckoo finches from mimicking certain host phenotypes that are currently favored by selection (e.g., the olive-green colored eggs laid by some tawny-flanked prinia, Prinia subflava, females). This illustrates an important cost of coding coevolved adaptations on the nonrecombining sex chromosome, which may impede further coevolutionary change by effectively reversing the advantages of sexual reproduction in antagonistic coevolution proposed by the Red Queen hypothesis.

Biogeographically marginal: Source of evolutionary novelties and future potential

Towards distribution margins, populations are thought to be genetically impoverished due to isolation and genetic drift acting in often small border populations. Here we analyse the hypothesis that contrary to expectations, populations towards the dry Nothofagus pumilio range are relicts of a past distribution, and thus hold comparable levels of genetic diversity than central ones using conserved chloroplast DNA (cpDNA) sequences. We sampled fresh leaf tissue from a total of 70 natural populations along a precipitation gradient in Northern Patagonia, Argentina, from central (N = 33), i. e. humid, to marginal (N = 37), i. e. dry, locations which were analysed by cpDNA sequencing and phylogeographic methods. We also analysed the fate of populations under global scenarios by ecological niche models. The analysis of a total of 186 cpDNA sequences yielded nine different haplotypes, eight and six of which were present in marginal and central regions, respectively. We identified four new haplotypes for the species, three were exclusive to the marginal region and one was also new for the Nothofagus subgenus. Haplotypes were latitudinally structured as previously documented, yet those from marginal and central regions diverged synchronically at ~3.5 Ma. Coalescence analyses yielded larger effective population sizes for marginal populations, except for the northernmost group, and divergence between regions occurred from early to late Pleistocene. Neutrality tests developed to infer past population size changes showed population stability for marginal and central regions yet current range retraction. Future distributions by ecological niche models predict population decay in both central and marginal regions with a stronger effect in the latter. Our results show that marginal populations are as genetically diverse and demographically stable as central ones and their genetic makeup may assure their long-lasting persistence. Unique variants and genetically-based adaptive traits of the former may be used as germplasm sources for restoration under forecasted droughts.

PseudoChecker: an integrated online platform for gene inactivation inference.

The rapid expansion of high-quality genome assemblies, exemplified by ongoing initiatives such as the Genome-10K and i5k, demands novel automated methods to approach comparative genomics. Of these, the study of inactivating mutations in the coding region of genes, or pseudogenization, as a source of evolutionary novelty is mostly overlooked. Thus, to address such evolutionary/genomic events, a systematic, accurate and computationally automated approach is required. Here, we present PseudoChecker, the first integrated online platform for gene inactivation inference. Unlike the few existing methods, our comparative genomics-based approach displays full automation, a built-in graphical user interface and a novel index, PseudoIndex, for an empirical evaluation of the gene coding status. As a multi-platform online service, PseudoChecker simplifies access and usability, allowing a fast identification of disruptive mutations. An analysis of 30 genes previously reported to be eroded in mammals, and 30 viable genes from the same lineages, demonstrated that PseudoChecker was able to correctly infer 97% of loss events and 95% of functional genes, confirming its reliability. PseudoChecker is freely available, without login required, at http://pseudochecker.ciimar.up.pt.

Population genetics of the banded coral shrimp, Stenopus hispidus ( ), in the Indonesian archipelago

The population genetics of the banded coral shrimp, Stenopus hispidus (Olivier, 1811) from the Indonesian Archipelago were investigated. We genotyped 387 individuals collected from 11 sampling locations throughout Indonesia at 15 microsatellite loci. Bayesian clustering methods revealed evidence of three genetically distinct clusters. F’ST and FST values are generally low, but significant. This was unexpected given the comparatively small geographic scale over which this survey was performed, approximately 2000km in an East to West orientation, even more so when accounting for the pan tropical distribution and long pelagic larval duration (210 days) of S. hispidus. Factors other than larval dispersal must be promoting population differentiation. In this case, genetic partitions appear to correspond to differing habitat types, possibly allowing selection to augment any oceanographic, geographic or biological barriers to gene flow, the resulting genetic differentiation is a source of evolutionary novelty and could facilitate reproductive isolation ultimately resulting in parapatric speciation.

Small Body Size Is Associated with Increased Aggression in the Solitary Sweat Bee Nomia melanderi (Hymenoptera, Halictidae)

Modifying ancestral regulatory mechanisms can be a source of evolutionary novelty. Bees in small-colony, dominance-based societies typically show a link between size and aggression: larger bees are more aggressive. This led to the hypothesis that this size-aggression link is a characteristic of ancestral solitary bees that has acquired a novel function in the evolutionary transition from solitary to social behavior. Here we test the central prediction of this hypothesis, that size is linked to aggression in an ancestrally solitary bee. We use the sweat bee Nomia melanderi (Hymenoptera, Halictidae) in the subfamily Nomiinae, which is sister to the social sweat bees, all of which are in the subfamily Halictinae. We measured aggression using a standardized behavioral assay (circle tube) in which two bees were placed together and allowed to interact. We used three treatments: size matched small bees, size matched large bees, and one large bee paired with one small bee. We found no link between ovary size and aggression, but because we used only reproductively active bees we may not have had sufficient variation to detect such a link. Across treatments, body size negatively correlated with aggression. There were no differences between large and small bees in the matched treatments, but in the mixed treatment, small bees were more aggressive than large bees. This supported our prediction of a size-aggression link, although the link was in the opposite direction seen in social bees. Moreover, our data show that even solitary bees can modulate their aggression in response to social context and highlight the importance of studying related solitary species to understand the evolutionary origins of sociality.

Integrating Networks, Phylogenomics, and Population Genomics for the Study of Polyploidy

Duplication events are regarded as sources of evolutionary novelty, but our understanding of general trends for the long-term trajectory of additional genomic material is still lacking. Organisms with a history of whole genome duplication (WGD) offer a unique opportunity to study potential trends in the context of gene retention and/or loss, gene and network dosage, and changes in gene expression. In this review, we discuss the prevalence of polyploidy across the tree of life, followed by an overview of studies investigating genome evolution and gene expression. We then provide an overview of methods in network biology, phylogenomics, and population genomics that are critical for advancing our understanding of evolution post-WGD, highlighting the need for models that can accommodate polyploids. Finally, we close with a brief note on the importance of random processes in the evolution of polyploids with respect to neutral versus selective forces, ancestral polymorphisms, and the formation of autopolyploids versus allopolyploids.

How does a widespread reef coral maintain a population in an isolated environment?

In a changing global environment, previously suboptimal habitats may become climate refuges for species. For instance, the ranges of some tropical reef corals are already expanding poleward. Understanding the demographic strategies by which isolated or marginal populations persist is therefore important, especially since such populations are often both vulnerable to local extinction and sources of evolutionary novelty. This study builds an integral projection model from individual-level demographic rates for a genetically isolated population of a reef coral, Plesiastrea versipora, in Sydney Harbour, Australia, in order to understand the population-level demographic characteristics allowing its persistence. We show that this population is thriving, with the potential to rapidly increase in benthic cover, due to high adult survivorship and at least sporadic high recruitment. Medium-sized colonies are the most important for long-term population viability due to their reproductive potential. Nonetheless, the population's persistence is sensitive to recruitment and growth rates, and protecting it from factors that affect these processes is likely to be crucial for its longer-term survival.

Mitogenomic and nuclear diversity in the Mulga Parrot of the Australian arid zone: cryptic subspecies and tests for selection

ABSTRACTThe Australian arid zone is well recognised as a source of evolutionary novelty and diversity. Roles for selection vs. drift in the region remain less understood. We surveyed mitogenomic diversity and genome-wide nuclear markers in the Mulga Parrot (Psephotellus varius) to add to phylogeographic data from arid zone species. We found structured diversity either side of the Flinders Ranges–Lake Eyre Basin (Eyrean barrier; net nucleotide divergence 1.92% for ND2). Coalescent analysis suggests that this arose during the mid-Pleistocene approximately 402 000 years ago. In both phylogroups, however, the mitogenome is under pervasive purifying selection. Purifying selection in the context of consistent environments either side of the Eyrean barrier may have maintained ancestral plumage and morphological traits, though in other plumage traits there is some plumage divergence that is geographically concordant with the phylogeographic structure. This leads to the essentially ‘cryptic’ genetic diversity uncovered here, despite indications of ongoing adaptation to aridity in P. varius as evidenced by increasing bill surface area (shown by earlier work to have increased relative to body size by 10.4% since 1871), a result we affirm here across the species as a whole. This study also demonstrates the utility of shallow ‘genome skimming’ sequencing for population analyses.

Introgressive hybridization and morphological transgression in the contact zone between two Mediterranean Solea species.

Hybrid zones provide natural experiments where new combinations of genotypes and phenotypes are produced. Studying the reshuffling of genotypes and remodeling of phenotypes in these zones is of particular interest to document the building of reproductive isolation and the possible emergence of transgressive phenotypes that can be a source of evolutionary novelties. Here, we specifically investigate the morphological variation patterns associated with introgressive hybridization between two species of sole, Solea senegalensis and Solea aegyptiaca. The relationship between genetic composition at nuclear loci and individual body shape variation was studied in four populations sampled across the hybrid zone located in northern Tunisia. A strong correlation between genetic and phenotypic variation was observed among all individuals but not within populations, including the two most admixed ones. Morphological convergence between parental species was observed close to the contact zone. Nevertheless, the samples taken closest to the hybrid zone also displayed deviant segregation of genotypes and phenotypes, as well as transgressive phenotypes. In these samples, deviant body shape variation could be partly attributed to a reduced condition index, and the distorted genetic composition was most likely due to missing allelic combinations. These results were interpreted as an indication of hybrid breakdown, which likely contributes to postmating reproductive isolation between the two species.

Host genotype–endosymbiont associations and their relationship with aphid parasitism at the field level

1. The relationship between endosymbionts and insects represent complex eco‐evolutionary interactions. Vertically transmitted endosymbionts can be a source of evolutionary novelty by conferring ecologically important traits to their insect hosts, such as protection against natural enemies. Host–endosymbiont associations could constitute an adaptive complex (holobiont) on which selective pressures present in the environment can act, being transferred to the next generation.2. Although several laboratory‐based studies have confirmed host genotype × symbiont interactions, few studies have been directed at those associations in the natural populations and their ability to protect themselves from parasitism pressure at the field level.3. A field‐based approach to study the aphid genotype–endosymbiont associations and its relationship with the total parasitism in the grain aphid Sitobion avenae was conducted. From the field study, experiments were carried out to study the defensive effect of the two most common facultative endosymbionts (Regiella insecticola and Hamiltonella defensa) present in S. avenae against one of the most important parasitoid species, Aphidius ervi.4. Evidence is presented here of a high specificity of the aphid clone–endosymbiont associations in the field; however, the field and experimental results here do not support a relationship between the aphid clone–endosymbiont associations and a proxy of total parasitism in S. avenae. These findings highlight the importance of particular host clone–endosymbiont couplings as a key factor in gaining an understanding of the coevolutionary dynamics of endosymbionts in nature and their effect on the invasive potential of pest insects.

Altitudinal gradients, plant hybrid zones and evolutionary novelty.

Altitudinal gradients are characterized by steep changes of the physical and biotic environment that present challenges to plant adaptation throughout large parts of the world. Hybrid zones may form where related species inhabit different neighbouring altitudes and can facilitate interspecific gene flow and potentially the breakdown of species barriers. Studies of such hybrid zones can reveal much about the genetic basis of adaptation to environmental differences stemming from changes in altitude and the maintenance of species divergence in the face of gene flow. Furthermore, owing to recombination and transgressive effects, such hybrid zones can be sources of evolutionary novelty. We document plant hybrid zones associated with altitudinal gradients and emphasize similarities and differences in their structure. We then focus on recent studies of a hybrid zone between two Senecio species that occur at high and low altitude on Mount Etna, Sicily, showing how adaptation to local environments and intrinsic selection against hybrids act to maintain it. Finally, we consider the potential of altitudinal hybrid zones for generating evolutionary novelty through adaptive introgression and hybrid speciation. Examples of homoploid hybrid species of Senecio and Pinus that originated from altitudinal hybrid zones are discussed.

Plasticity of ontogenetic trajectories in cyprinids: a source of evolutionary novelties

Research in evolutionary developmental (evo-devo) biology is making an increasingly important contribution to our understanding of the molecular mechanisms underlying the establishment of complex morphological traits. Deciphering the ontogenetic trajectories leading to the differentiation of sister species (and the existence of hybrids) is a new challenge in our understanding of speciation processes. In the present study, we characterized the ontogenetic trajectory of lower lip morphology in two cyprinid species and their hybrids. Chondrostoma toxostoma has an arched lower lip and a generalist diet. Chondrostoma nasus has a straight lower lip and a specialist diet. An analysis of 99 C. toxostoma ,9 9C. nasus and 25 first-generation (F1) hybrid individuals demonstrated that the difference between arched and straight lip morphology was found to depend strongly on the height/width ratio of the lower lip. A comparison of the ontogenetic trajectories of these morphometric traits showed that the height of the lower lip was isometric to body length in both species, whereas developmental changes involving an acceleration and a hypermorphosis of the widening of the lower lip led to a straight lip morphology in C. nasus. F1 hybrids were characterized by an extreme phenotype resulting from a rate of lower lip widening slower than that in the two parent species. Therefore, we rejected a codominance hypothesis and concluded that the first stage of hybridization provides the foundations of evolutionary novelty. These results have important evolutionary implications because lower lip shape is linked to dietary behaviour in many fish species. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 342‐355. ADDITIONAL KEYWORDS: Cyprinidae ‐ heterochrony ‐ hybridization ‐ hypermorphosis ‐ jaw shape ‐ Procrustes analysis.

An inverse latitudinal gradient of diversity of peracarid crustaceans along the Pacific Coast of South America: out of the deep south

Aim To understand the ecological and historical/evolutionary processes underlying an inverse latitudinal gradient of richness (LGR) using crustacean peracarid species as a model group. Location The Pacific coast of South America, along the Chilean coast between 18° S and 56° S. Methods The LGR was evaluated using a dataset including 320 marine peracarid species reported for the coasts of Chile. Five ecological hypotheses invoking a relationship between species richness and present-day conditions were tested: species–energy, species–area, Rapoport rescue effect, mid-domain geometric constraint and niche breadth. Historical/evolutionary hypotheses (i.e. biogeographic conservatism, and diversification rates) were indirectly tested by analysing the latitudinal variation in the taxonomic distinctness, the taxonomic conservatism of the midpoint of the latitudinal range and the degree of nestedness at different taxonomic levels. Results Richness increased poleward, varying approximately eightfold, following an inverse LGR coupled with an increase in bathymetric distribution. Overall this inverse LGR seems robust to uncertainties in the completeness of the species inventory. We found support for only two of the five ecological hypotheses tested: species–area and Rapoport rescue effect. Historical/evolutionary hypotheses seemed important in structuring the richness pattern, as indicated by the higher taxonomic distinctness in the southern region, the strong taxonomic inertia in the mean range size and the high degree of nestedness of assemblages at different taxonomic levels. Conclusions When combined, these results underscore the importance of longterm processes and historical/evolutionary explanations for the inverse LGR, conceptualized in what we term the ‘out of the deep south’ hypothesis that involves the effects of both biogeographic niche conservatism and evolutionary rates. We propose that the southern region may be a source of evolutionary novelties and/or exhibit higher diversification rates (i.e. higher speciation/lower extinction rates). Furthermore, phylogenetic conservatism of latitudinal range may limit the geographic expansion of these new taxa towards the depauperated northern region.

Shadow Enhancers as a Source of Evolutionary Novelty

Some developmentally important genes can be regulated via two enhancers, one located nearby and the other, a "shadow" enhancer, 10 to 20 kilobases away.

Symbiosis

Symbiosis

Hybridization as a source of evolutionary novelty: leaf shape in a Hawaiian composite

Hybridization is increasingly recognized as a significant creative force in evolution. Interbreeding among species can lead to the creation of novel genotypes and morphologies that lead to adaptation. On the Hawaiian island of O'ahu, populations of two species of plants in the endemic genus Lipochaeta grow at similar elevations in the northern Wai'anae Mountains. These two species represent extremes of the phenotypic distribution of leaf shape: the leaves of Lipochaeta tenuifolia individuals are compound and highly dissected while leaves of L. tenuis are simple. Based primarily on leaf shape morphology, a putative hybrid population of Lipochaeta located at Pu'u Kawiwi was identified. Individuals in this population exhibit a range of leaf shapes intermediate in varying degrees between the leaf shapes of the putative parental species. We analyzed individuals from pure populations of L. tenuifolia, L. tenuis and the putative hybrids using 133 AFLP markers. Genetic analysis of these neutral markers provided support for the hybrid origin of this population. The correlation between genetic background and leaf morphology in the hybrids suggested that the genome of the parental species with simple leaves might have significantly contributed to the evolution of a novel, compound leaf morphology.

Symbiotic origin of a novel actin gene in the cryptophyte Pyrenomonas helgolandii.

Cryptophytes are photosynthetic protists that have acquired their plastids through the secondary symbiotic uptake of a red alga. A remarkable feature of cryptophytes is that they maintain a reduced form of the red algal nucleus, the nucleomorph, between the second and third plastid membranes (periplastidial compartment; PC). The nucleomorph is thought to be a transition state in the evolution of secondary plastids, with this genome ultimately being lost when photosynthesis comes under full control of the "host" nucleus (e.g., as in heterokonts, haptophytes, and euglenophytes). Genes presently found in the nucleomorph seem to be restricted to those involved in its own maintenance and to that of the plastid; other genes were lost as the endosymbiont was progressively reduced to its present state. Surprisingly, we found that the cryptophyte Pyrenomonas helgolandii possesses a novel type of actin gene that originated from the nucleomorph genome of the symbiont. Our results demonstrate for the first time that secondary symbionts can contribute genes to the host lineage which are unrelated to plastid function. These genes are akin to the products of gene duplication or lateral transfer and provide a source of evolutionary novelty that can significantly increase the genetic diversity of the host lineage. We postulate that this may be a common phenomenon in algae containing secondary plastids that has yet to be fully appreciated due to a dearth of evolutionary studies of nuclear genes in these taxa.