Spatial and temporal patterns of genetic diversity in Bombus terrestris populations of the Iberian Peninsula and their conservation implications

The bumblebee Bombus terrestris is used worldwide for crop pollination. Despite its positive impact on crop yield, it has become a widespread threat to biodiversity due to its interactions with local bumblebee populations. Commercial subspecies introduced to the Iberian Peninsula since the 1990s without any regulation have colonized the environment, with evidence of naturalization and introgression with the endemic subspecies Bombus terrestris lusitanicus. We have used mitochondrial and nuclear genetic data to describe the current genetic diversity of the Iberian population and to estimate the expansion of commercial bumblebees. Samples from the natural distribution range of the commercial subspecies, the natural intergradation area between the two subspecies and from a period prior to the use of commercial colonies (i.e., before the 1990s) have been used for comparison. Our results show that the mitochondrial haplotype of the commercial breeds has spread throughout the territory, which, together with subtle changes observed in the nuclear genetic diversity of the populations, indicates that hybridization and consequent introgression are occurring in most of the peninsula. It is, therefore, necessary to improve the existing legislation concerning the management and exportation of commercial bumblebees to conserve locally adapted populations.

Ancient mitogenomes unravel massive genetic diversity loss during near extinction of Alpine ibex

Population bottlenecks can have dramatic consequences for the health and long-term survival of a species. A recent bottleneck event can also largely obscure our understanding of standing variation prior to the contraction. Historic population sizes can be modeled based on extant genomics, however uncertainty increases with the severity of the bottleneck. Integrating ancient genomes provides a powerful complement to retrace the evolution of genetic diversity through population fluctuations. Here, we recover 15 high-quality mitogenomes of the once nearly extinct Alpine ibex spanning 8601 BP to 1919 CE and combine these with 60 published modern genomes. Coalescent demography simulations based on modern genomes indicate population fluctuations matching major climatic change over the past millennia. Using ancient genomes, we show that mitochondrial haplotype diversity has been reduced to a fifth of the pre-bottleneck diversity with several highly differentiated mitochondrial lineages having co-existed historically. The main collapse of mitochondrial diversity coincided with human settlement expansions in the Middle Ages. The near extinction severely reduced the mitochondrial diversity. After recovery, one lineage was spread and nearly fixed across the Alps due to recolonization efforts. Contrary to expectations, we show that a second ancestral mitochondrial lineage has survived in an isolated population further south. Our study highlights that a combined approach integrating genomic data of ancient, historic and extant populations unravels major long-term population fluctuations.

Wolbachia-driven selective sweep in a range expanding insect species

Background Evolutionary processes can cause strong spatial genetic signatures, such as local loss of genetic diversity, or conflicting histories from mitochondrial versus nuclear markers. Investigating these genetic patterns is important, as they may reveal obscured processes and players. The maternally inherited bacterium Wolbachia is among the most widespread symbionts in insects. Wolbachia typically spreads within host species by conferring direct fitness benefits, and/or by manipulating its host reproduction to favour infected over uninfected females. Under sufficient selective advantage, the mitochondrial haplotype associated with the favoured maternally-inherited symbiotic strains will spread (i.e. hitchhike), resulting in low mitochondrial genetic variation across the host species range. Method The common bluetail damselfly (Ischnura elegans: van der Linden, 1820) has recently emerged as a model organism for genetics and genomic signatures of range expansion during climate change. Although there is accumulating data on the consequences of such expansion on the genetics of I. elegans, no study has screened for Wolbachia in the damselfly genus Ischnura. Here, we present the biogeographic variation in Wolbachia prevalence and penetrance across Europe and Japan (including samples from 17 populations), and from close relatives in the Mediterranean area (i.e. I. genei: Rambur, 1842; and I. saharensis: Aguesse, 1958). Results Our data reveal (a) multiple Wolbachia-strains, (b) potential transfer of the symbiont through hybridization, (c) higher infection rates at higher latitudes, and (d) reduced mitochondrial diversity in the north-west populations, indicative of hitchhiking associated with the selective sweep of the most common strain. We found low mitochondrial haplotype diversity in the Wolbachia-infected north-western European populations (Sweden, Scotland, the Netherlands, Belgium, France and Italy) of I. elegans, and, conversely, higher mitochondrial diversity in populations with low penetrance of Wolbachia (Ukraine, Greece, Montenegro and Cyprus). The timing of the selective sweep associated with infected lineages was estimated between 20,000 and 44,000 years before present, which is consistent with the end of the last glacial period about 20,000 years. Conclusions Our findings provide an example of how endosymbiont infections can shape spatial variation in their host evolutionary genetics during postglacial expansion. These results also challenge population genetic studies that do not consider the prevalence of symbionts in many insects, which we show can impact geographic patterns of mitochondrial genetic diversity.

Defensive Behavior and Morphometric Variation in Apis mellifera Colonies From Two Different Agro-Ecological Zones of North-Western Argentina

European lineages of Apis mellifera were first introduced into America for beekeeping purposes. A subsequent introduction and accidental release of A. m. scutellata resulted in hybridization events that gave rise to Africanized populations that rapidly spread throughout the continent. In Argentina, Africanized honey bees (AHBs) have been mostly detected in northern regions of the territory, and represent a valuable genetic resource for the selection of stocks with advantageous characteristics for beekeeping. The objective of the present study was to profile honey bee colonies of wild origin with potential beneficial traits for apiculture using morphological, molecular and behavioral traits. Honey bee colonies chosen for evaluation were located in two different agro-ecological regions in north-western Argentina (Tucumán province): The Chaco Depressed Plain (Leales apiary) and the Piedmont (Famaillá apiary). Each apiary was surveyed three times during the 2017–2018 season (mid-season, wintertime, and early spring) for: brood population, phoretic Varroa level and defensive behavior (run, fly, sting, and hang). At the midpoint of the beekeeping season colonies were also characterized by morphometry (45 variables) and mitochondrial haplotypes (COI–COII intergenic region). Apiaries studied showed similar patterns throughout the beekeeping season, for most of the characteristics monitored. However, significant variation in defensive behavior parameters was found between apiaries at the different times of evaluation. Twelve of 45 morphometric variables also showed significant differences between apiaries. The mitochondrial haplotype analysis revealed a high representation of African A4 and A1 haplotypes (91%) in both apiaries. Haplotype variation was associated with morphometric and behavioral traits. Multivariate analyses [principal component analysis (PCA) and principal coordinate analysis (PCoA)] including morphometric and behavior variables explained 65.3% (PCA) and 48.1% (PCoA) of the variability observed between colonies in the first two components. Several morphometric parameters and “fly” behavior were mainly associated with the separation of the colonies. The results from this study point to a possible association between morphometric and behavioral variation and the adaptation of honey bee colonies to differential agro-ecological conditions. We discuss how the detected variation between apiaries can be used for the selection and preservation of honey bee ecotypes in regional breeding programs.

Mitochondrial introgression by ancient admixture between two distant lacustrine fishes in Sulawesi Island

Sulawesi, an island located in a biogeographical transition zone between Indomalaya and Australasia, is famous for its high levels of endemism. Ricefishes (family Adrianichthyidae) are an example of taxa that have uniquely diversified on this island. It was demonstrated that habitat fragmentation due to the Pliocene juxtaposition among tectonic subdivisions of this island was the primary factor that promoted their divergence; however, it is also equally probable that habitat fusions and resultant admixtures between phylogenetically distant species may have frequently occurred. Previous studies revealed that some individuals of Oryzias sarasinorum endemic to a tectonic lake in central Sulawesi have mitochondrial haplotypes that are similar to the haplotypes of O. eversi, which is a phylogenetically related but geologically distant (ca. 190 km apart) adrianichthyid endemic to a small fountain. In this study, we tested if this reflects ancient admixture of O. eversi and O. sarasinorum. Population genomic analyses of genome-wide single-nucleotide polymorphisms revealed that O. eversi and O. sarasinorum are substantially reproductively isolated from each other. Comparison of demographic models revealed that the models assuming ancient admixture from O. eversi to O. sarasinorum was more supported than the models assuming no admixture; this supported the idea that the O. eversi-like mitochondrial haplotype in O. sarasinorum was introgressed from O. eversi. This study is the first to demonstrate ancient admixture of lacustrine or pond organisms in Sulawesi beyond 100 km. The complex geological history of this island enabled such island-wide admixture of lacustrine organisms, which usually experience limited migration.

Hereditary symbionts and mitochondria: distribution in insect populations and quasi-linkage of genetic markers

Maternal transmission ensures the joint transmission and simultaneous presence in populations of individuals with certain variants of the bacterial symbiont and host mitochondrial DNA. Such “quasi-linkage” of cytoplasmic genomes among insects and other arthropods is widespread. The symbiont acts as a “driver” of mitochondria and the obvious biological consequence is the spread of the “linked” mitochondrial haplotype in the population, which itself does not have increased selective value to the organism. Examples of such indirect selective mitochondrial sweep in insects are discussed, as well as biological consequences of this phenomenon and mechanisms of increasing the frequency of symbiont-infected individuals in the population.

Insights into the Mitochondrial and Nuclear Genome Diversity of Two High Yielding Strains of Laying Hens

Mitochondria are essential components of eukaryotes as they are involved in several organismic key processes such as energy production, apoptosis and cell growth. Despite their importance for the metabolism and physiology of all eukaryotic organisms, the impact of mitochondrial haplotype variation has only been studied for very few species. In this study we sequenced the mitochondrial genome of 180 individuals from two different strains of laying hens. The resulting haplotypes were combined with performance data such as body weight, feed intake and phosphorus utilization to assess their influence on the hens in five different life stages. After detecting a surprisingly low level of genetic diversity, we investigated the nuclear genetic background to estimate whether the low mitochondrial diversity is representative for the whole genetic background of the strains. Our results highlight the need for more in-depth investigation of the genetic compositions and mito-nuclear interaction in individuals to elucidate the basis of phenotypic performance differences. In addition, we raise the question of how the lack of mitochondrial variation developed, since the mitochondrial genome represents genetic information usually not considered in breeding approaches.

Wolbachia-driven selective sweep in a range expanding insect species

Background Evolutionary processes can cause strong spatial genetic signatures, such as local loss of genetic diversity, or conflicting histories from mitochondrial versus nuclear markers. Investigating these genetic patterns is important, as they may reveal obscured processes and players. The maternally inherited bacterium Wolbachia is among the most widespread symbionts in insects. Wolbachia typically spreads within host species by conferring direct fitness benefits, or by manipulating its host reproduction to favour infected over uninfected females. Under sufficient selective advantage, the mitochondrial haplotype associated with the favoured symbiotic strains will spread (i.e. hitchhike), resulting in low mitochondrial genetic variation across the host species range. The common bluetail damselfly (Ischnura elegans: van der Linden, 1820) has recently emerged as a model organism of the genetics and genomic signatures of range expansion during climate change. Although there is accumulating data on the consequences of such expansion on the genetic of I. elegans, no study has screened for Wolbachia in the damselfly genus Ischnura. Here, we present the biogeographic variation in Wolbachia prevalence and penetrance in 17 I. elegans populations across Europe and Japan, and from close relatives in the Mediterranean area (i.e. I. genei: Rambur, 1842; and I. saharensis: Aguesse, 1958). Results Our data reveal (a) multiple Wolbachia-strains, (b) potential transfer of the symbiont through hybridization, (c) higher infection rates at higher latitudes, and (d) reduced mitochondrial diversity in the north-west populations, indicative of hitchhiking associated with the selective sweep of the most common strain. We found low mitochondrial haplotype diversity in the Wolbachia-infected north-western European populations (Sweden, Scotland, the Netherlands, Belgium, France and Italy) of I. elegans, and, conversely, higher mitochondrial diversity in populations with low penetrance of Wolbachia (Ukraine, Greece, Montenegro and Cyprus). The timing of the selective sweep associated with infected lineages was estimated between 20 000 to 44 000 years before present, which is consistent with the end of the last glacial period about 20 000 ya. Conclusions Our findings provide an example of how endosymbiont infections ca shape spatial variation in their host evolutionary genetics during postglacial expansion. These results also challenge population genetic studies that do not consider the prevalence of symbionts in many insects, which can impact geographic patterns of mitochondrial genetic diversity.

Sexually antagonistic evolution of mitochondrial and nuclear linkage

Across eukaryotes, genes encoding bioenergetic machinery are located in both mitochondrial and nuclear DNA, and incompatibilities between the two genomes can be devastating. Mitochondria are often inherited maternally, and theory predicts sex-specific fitness effects of mitochondrial mutational diversity. Yet how evolution acts on linkage patterns between mitochondrial and nuclear genomes is poorly understood. Using novel mito-nuclear population genetic models, we show that the interplay between nuclear and mitochondrial genes maintains mitochondrial haplotype diversity within populations, and it selects both for sex-independent segregation of mitochondrion-interacting genes and for paternal leakage. These effects of genetic linkage evolution can eliminate male-harming fitness effects of mtDNA mutational diversity. With maternal mitochondrial inheritance, females maintain a tight mitochondrial-nuclear match, but males accumulate mismatch mutations because of the weak statistical associations between the two genomic components. Sex-independent segregation of mitochondria-interacting loci improves the mito-nuclear match. In a sexually antagonistic evolutionary process, male nuclear alleles evolve to increase the rate of recombination, while females evolve to suppress it. Paternal leakage of mitochondria can evolve as an alternative mechanism to improve the mito-nuclear linkage. Our modelling framework provides an evolutionary explanation for the observed paucity of mitochondrion-interacting genes on mammalian sex chromosomes and for paternal leakage in protists, plants, fungi, and some animals.

Wolbachia-driven selective sweep in a range expanding insect species

BackgroundEvolutionary processes can cause strong spatial genetic signatures, such as local loss of genetic diversity, or conflicting histories from mitochondrial versus nuclear markers. Investigating these genetic patterns is important, as they may reveal obscured processes and players. The maternally inherited bacterium Wolbachia is among the most widespread symbionts in insects. Wolbachia typically spreads within host species by conferring direct fitness benefits, or by manipulating its host reproduction to favour infected over uninfected females. Under sufficient selective advantage, the mitochondrial haplotype associated with the favoured symbiotic strains will spread (i.e. hitchhike), resulting in low mitochondrial genetic variation across the host species range. The common bluetail damselfly (Ischnura elegans: van der Linden, 1820) has recently emerged as a model organism of the genetics and genomic signatures of range expansion during climate change. Although there is accumulating data on the consequences of such expansion on the genetic of I. elegans, no study has screened for Wolbachia in the damselfly genus Ischnura. Here, we present the biogeographic variation in Wolbachia prevalence and penetrance in 17 I. elegans populations across Europe and Japan, and from close relatives in the Mediterranean area (i.e. I. genei: Rambur, 1842; and I. saharensis: Aguesse, 1958). ResultsOur data reveal (a) multiple Wolbachia-strains, (b) potential transfer of the symbiont through hybridization, (c) higher infection rates at higher latitudes, and (d) reduced mitochondrial diversity in the north-west populations, indicative of hitchhiking associated with the selective sweep of the most common strain. We found low mitochondrial haplotype diversity in the Wolbachia-infected north-western European populations (Sweden, Scotland, the Netherlands, Belgium, France and Italy) of I. elegans, and, conversely, higher mitochondrial diversity in populations with low penetrance of Wolbachia (Ukraine, Greece, Montenegro and Cyprus). The timing of the selective sweep associated with infected lineages was estimated between 20 000 to 44 000 years before present, which is consistent with the end of the last glacial period about 20 000 ya. ConclusionsOur findings provide an example of how endosymbiont infections ca shape spatial variation in their host evolutionary genetics during postglacial expansion. These results also challenge population genetic studies that do not consider the prevalence of symbionts in many insects, which can impact geographic patterns of mitochondrial genetic diversity.