Patterns of reproductive isolation in a haplodiploid mite, Amphitetranychus viennensis: prezygotic isolation, hybrid inviability and hybrid sterility

Abstract Background Evolution of reproductive isolation is an important process, generating biodiversity and driving speciation. To better understand this process, it is necessary to investigate factors underlying reproductive isolation through various approaches but also in various taxa. Previous studies, mainly focusing on diploid animals, supported the prevalent view that reproductive barriers evolve gradually as a by-product of genetic changes accumulated by natural selection by showing a positive relationship between the degree of reproductive isolation and genetic distance. Haplodiploid animals are expected to generate additional insight into speciation, but few studies investigated the prevalent view in haplodiploid animals. In this study, we investigate whether the relationship also holds in a haplodiploid spider mite, Amphitetranychus viennensis (Zacher). Results We sampled seven populations of the mite in the Palaearctic region, measured their genetic distance (mtDNA) and carried out cross experiments with all combinations. We analyzed how lack of fertilization rate (as measure of prezygotic isolation) as well as hybrid inviability and hybrid sterility (as measures of postzygotic isolation) varies with genetic distance. We found that the degree of reproductive isolation varies among cross combinations, and that all three measures of reproductive isolation have a positive relationship with genetic distance. Based on the mtDNA marker, lack of fertilization rate, hybrid female inviability and hybrid female sterility were estimated to be nearly complete (99.0–99.9% barrier) at genetic distances of 0.475–0.657, 0.150–0.209 and 0.138–0.204, respectively. Conclusions The prevalent view on the evolution of reproductive barriers is supported in the haplodiploid spider mite we studied here. According to the estimated minimum genetic distance for total reproductive isolation in parent population crosses in this and previous studies, a genetic distance of 0.152–0.210 in mtDNA (COI) appears required for speciation in spider mites. Due to a lack of hybrid males, we could not address Haldane’s rule, which can be extended to haplodiploids, even though we focused on a young diverging group of spider mites. Our results highlight the importance of cytonuclear interactions for reproductive isolation in haplodiploid spider mites.

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Patterns of reproductive isolation in a haplodiploid mite, Amphitetranychus viennensis: prezygotic isolation, hybrid inviability and hybrid sterility

BMC Ecology and Evolution ◽

10.1186/s12862-021-01896-5 ◽

2021 ◽

Vol 21 (1) ◽

Author(s):

Yukie Sato ◽

Satoshi Fujiwara ◽

Martijn Egas ◽

Tomoko Matsuda ◽

Tetsuo Gotoh

Keyword(s):

Reproductive Isolation ◽

Genetic Distance ◽

Spider Mite ◽

Hybrid Sterility ◽

Fertilization Rate ◽

Spider Mites ◽

Reproductive Barriers ◽

Hybrid Female ◽

Hybrid Inviability ◽

Prezygotic Isolation

Abstract Background Evolution of reproductive isolation is an important process, generating biodiversity and driving speciation. To better understand this process, it is necessary to investigate factors underlying reproductive isolation through various approaches but also in various taxa. Previous studies, mainly focusing on diploid animals, supported the prevalent view that reproductive barriers evolve gradually as a by-product of genetic changes accumulated by natural selection by showing a positive relationship between the degree of reproductive isolation and genetic distance. Haplodiploid animals are expected to generate additional insight into speciation, but few studies investigated the prevalent view in haplodiploid animals. In this study, we investigate whether the relationship also holds in a haplodiploid spider mite, Amphitetranychus viennensis (Zacher). Results We sampled seven populations of the mite in the Palaearctic region, measured their genetic distance (mtDNA) and carried out cross experiments with all combinations. We analyzed how lack of fertilization rate (as measure of prezygotic isolation) as well as hybrid inviability and hybrid sterility (as measures of postzygotic isolation) varies with genetic distance. We found that the degree of reproductive isolation varies among cross combinations, and that all three measures of reproductive isolation have a positive relationship with genetic distance. Based on the mtDNA marker, lack of fertilization rate, hybrid female inviability and hybrid female sterility were estimated to be nearly complete (99.0–99.9% barrier) at genetic distances of 0.475–0.657, 0.150–0.209 and 0.145–0.210, respectively. Besides, we found asymmetries in reproductive isolation. Conclusions The prevalent view on the evolution of reproductive barriers is supported in the haplodiploid spider mite we studied here. According to the estimated minimum genetic distance for total reproductive isolation in parent population crosses in this study and previous work, a genetic distance of 0.15–0.21 in mtDNA (COI) appears required for speciation in spider mites. Variations and asymmetries in the degree of reproductive isolation highlight the importance of reinforcement of prezygotic reproductive isolation through incompatibility and the importance of cytonuclear interactions for reproductive isolation in haplodiploid spider mites.

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Wolbachia and host intrinsic reproductive barriers contribute additively to post-mating isolation in spider mites

10.1101/2020.06.29.178699 ◽

2020 ◽

Cited By ~ 1

Author(s):

Miguel Alfredo Cruz ◽

Sara Magalhaes ◽

Elio Sucena ◽

Flore Zele

Keyword(s):

Reproductive Isolation ◽

Spider Mite ◽

Cytoplasmic Incompatibility ◽

Hybrid Sterility ◽

Spider Mites ◽

Reproductive Barriers ◽

Hybrid Breakdown ◽

F1 Hybrid ◽

Hybrid Production ◽

Relative Contribution

Wolbachia are widespread maternally-inherited bacteria suggested to play a role in arthropod host speciation through induction of cytoplasmic incompatibility, but this hypothesis remains controversial. Most studies addressing Wolbachia-induced incompatibilities concern closely-related populations, which are intrinsically compatible. Here, we used three populations of two genetically differentiated colour forms of the haplodiploid spider mite Tetranychus urticae to dissect the interaction between Wolbachia-induced and host-associated incompatibilities, and to assess their relative contribution to post-mating isolation. We found that these two sources of incompatibility act through different mechanisms in an additive fashion. Host-associated incompatibility contributes 1.5 times more than Wolbachia-induced incompatibility in reducing hybrid production, the former through an overproduction of haploid sons at the expense of diploid daugters (ca. 75% decrease) and the latter by increasing the embryonic mortality of daughters (by ca. 49%). Furthermore, regardless of cross direction, we observed near-complete F1 hybrid sterility and complete F2 hybrid breakdown between populations of the two forms, but that Wolbachia did not contribute to this outcome. This study identifies the mechanistic independence and additive nature of host-intrinsic and Wolbachia-induced sources of isolation. It suggests that Wolbachia could drive reproductive isolation in this system, thereby potentially affecting host differentiation and distribution in the field.

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When acting as a reproductive barrier for sympatric speciation, hybrid sterility can only be primary

Biological Journal of the Linnean Society ◽

10.1093/biolinnean/blz135 ◽

2019 ◽

Vol 128 (4) ◽

pp. 779-788 ◽

Cited By ~ 2

Author(s):

Donald R Forsdyke

Keyword(s):

Hybrid Sterility ◽

Sympatric Speciation ◽

The Other ◽

Reproductive Barriers ◽

Evolutionary Time ◽

Hybrid Inviability ◽

Prezygotic Isolation ◽

Microscopic Scale ◽

A New Species

Abstract Animal gametes unite to form a zygote that develops into an adult with gonads that, in turn, produce gametes. Interruption of this germinal cycle by prezygotic or postzygotic reproductive barriers can result in two cycles, each with the potential to evolve into a new species. When the speciation process is complete, members of each species are fully reproductively isolated from those of the other. During speciation a primary barrier may be supported and eventually superceded by a later-appearing secondary barrier. For those holding certain cases of prezygotic isolation to be primary (e.g. elephant cannot copulate with mouse), the onus is to show that they had not been preceded over evolutionary time by periods of postzygotic hybrid inviability (genically determined) or sterility (genically or chromosomally determined). Likewise, the onus is upon those holding cases of hybrid inviability to be primary (e.g. Dobzhansky–Muller epistatic incompatibilities) to show that they had not been preceded by periods, however brief, of hybrid sterility. The latter, when acting as a sympatric barrier causing reproductive isolation, can only be primary. In many cases, hybrid sterility may result from incompatibilities between parental chromosomes that attempt to pair during meiosis in the gonad of their offspring (Winge-Crowther-Bateson incompatibilities). While such incompatibilities have long been observed on a microscopic scale, there is growing evidence for a role of dispersed finer DNA sequence differences (i.e. in base k-mers).

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The Genetics of Reproductive Isolation in the Drosophila simulans Clade: X vs. Autosomal Effects and Male vs. Female Effects

Genetics ◽

10.1093/genetics/143.3.1243 ◽

1996 ◽

Vol 143 (3) ◽

pp. 1243-1255 ◽

Cited By ~ 1

Author(s):

Hope Hollocher ◽

Chug-I Wu

Keyword(s):

Reproductive Isolation ◽

Male Sterility ◽

X Chromosome ◽

Hybrid Sterility ◽

Drosophila Simulans ◽

Female Sterility ◽

Hybrid Male ◽

Hybrid Female ◽

Hybrid Male Sterility ◽

Hybrid Inviability

Abstract A strong effect of homozygous autosomal regions on reproductive isolation was found for crosses between the species in the Drosophila simulans clade. Second chromosome regions were introgressed from D. mauritiana and D. sechellia into D. simulans and tested for their homozygous effects on hybrid male and hybrid female sterility and inviability. Most introgressions are fertile as heterozygotes, yet produce sterile male offspring when made homozygous. The density of homozygous autosomal factors contributing to hybrid male sterility is comparable to the density of X chromosome factors for this level of resolution. Female sterility was also revealed, yet the disparity between male and female levels of sterility was great, with male sterility being up to 23 times greater than female sterility. Complete hybrid inviability was also associated with some regions of the second chromosome, yet there were no strong sex differences. In conclusion, we find no evidence to support a strong X chromosome bias in the evolution of hybrid sterility or inviability but do find a very strong sex bias in the evolution of hybrid sterility. In light of these findings, we reevaluate the current models proposed to explain the genetic pattern of reproductive isolation.

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Postzygotic Isolation Evolves before Prezygotic Isolation between Fresh and Saltwater Populations of the Rainwater Killifish, Lucania parva

International Journal of Evolutionary Biology ◽

10.1155/2012/523967 ◽

2012 ◽

Vol 2012 ◽

pp. 1-11 ◽

Cited By ~ 13

Author(s):

Genevieve M. Kozak ◽

Arthur B. Rudolph ◽

Beatrice L. Colon ◽

Rebecca C. Fuller

Keyword(s):

Reproductive Isolation ◽

Fresh Water ◽

Salt Water ◽

Postzygotic Isolation ◽

Hybrid Inviability ◽

Prezygotic Isolation ◽

Divergent Natural Selection ◽

Postzygotic Barriers ◽

Species Population ◽

Stable Populations

Divergent natural selection has the potential to drive the evolution of reproductive isolation. The euryhaline killifish Lucania parva has stable populations in both fresh water and salt water. Lucania parva and its sister species, the freshwater L. goodei, are isolated by both prezygotic and postzygotic barriers. To further test whether adaptation to salinity has led to the evolution of these isolating barriers, we tested for incipient reproductive isolation within L. parva by crossing freshwater and saltwater populations. We found no evidence for prezygotic isolation, but reduced hybrid survival indicated that postzygotic isolation existed between L. parva populations. Therefore, postzygotic isolation evolved before prezygotic isolation in these ecologically divergent populations. Previous work on these species raised eggs with methylene blue, which acts as a fungicide. We found this fungicide distorts the pattern of postzygotic isolation by increasing fresh water survival in L. parva, masking species/population differences, and underestimating hybrid inviability.

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Patterns of hybrid seed inviability in perennials of the Mimulus guttatus sp. complex reveal a potential role of parental conflict in reproductive isolation

10.1101/458315 ◽

2018 ◽

Cited By ~ 1

Author(s):

Jenn M. Coughlan ◽

Maya Wilson Brown ◽

John H. Willis

Keyword(s):

Resource Allocation ◽

Reproductive Isolation ◽

Potential Role ◽

Rapid Evolution ◽

Hybrid Seed ◽

Parental Conflict ◽

Reproductive Barriers ◽

Hybrid Inviability ◽

Parent Of Origin

SummaryGenomic conflicts may play a central role in the evolution of reproductive barriers. Theory predicts that early-onset hybrid inviability may stem from conflict between parents for resource allocation to offspring. Here we describe M. decorus; a group of cryptic species within the M. guttatus species complex that are largely reproductively isolated by hybrid seed inviability (HSI). HSI between M. guttatus and M. decorus is common and strong, but populations of M. decorus vary in the magnitude and directionality of HSI with M. guttatus. Patterns of HSI between M. guttatus and M. decorus, as well as within M. decorus conform to the predictions of parental conflict: (1) reciprocal F1s exhibit size differences and parent-of-origin specific endosperm defects, (2) the extent of asymmetry between reciprocal F1 seed size is correlated with asymmetry in HSI, and (3) inferred differences in the extent of conflict predict the extent of HSI between populations. We also find that HSI is rapidly evolving, as populations that exhibit the most HSI are each others’ closest relative. Lastly, while all populations are largely outcrossing, we find that the differences in the inferred strength of conflict scale positively with π, suggesting that demographic or life history factors other than mating system may also influence the rate of parental conflict driven evolution. Overall, these patterns suggest the rapid evolution of parent-of-origin specific resource allocation alleles coincident with HSI within and between M. guttatus and M. decorus. Parental conflict may therefore be an important evolutionary driver of reproductive isolation.

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Advances in the genetics of reproductive isolation in Drosophila

Genome ◽

10.1139/g89-036 ◽

1989 ◽

Vol 31 (1) ◽

pp. 211-220 ◽

Cited By ~ 17

Author(s):

E. Zouros

Keyword(s):

Reproductive Isolation ◽

Molecular Mechanisms ◽

Hybrid Sterility ◽

Genetic Material ◽

Future Generation ◽

Major Advance ◽

Hybrid Inviability ◽

Mating Preferences ◽

Morphological Differences ◽

Made In

Speciation genetics is defined as the study of genetic events and processes that differentiate the probabilities that genetic material from individual members of a population will co-occur in individuals of some future generation. It follows that phenotypic attributes that contribute to this differentiation of probabilities (e.g., mating preferences, sterility, or infertility of individuals from certain types of matings) constitute the phenotype of speciation, and genetic loci that may affect these phenotypic attributes can be considered as speciation genes. The literature on genetic differences between hybridizable species of Drosophila that are responsible for morphological differences, mating preferences, hybrid inviability, and hybrid sterility are reviewed with special reference to the species pair D. mojavensis – D. arizonensis. The case for the involvement of karyotypic changes in speciation in rodents is briefly discussed. It is concluded that no major advance has been made in the speciation genetics of Drosophila since Dobzhansky initiated the field 40 years ago. Yet, the identification of several gene loci that cause hybrid inviability or sterility may open the way to the understanding of reproductive isolation at the molecular level. It is not clear whether this approach will lead to general molecular mechanisms underlying the speciation process.Key words: speciation genetics, hybrid sterility, reproductive isolation, Drosophila.

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Stability and Resiliency of Biological Control of the Twospotted Spider Mite (Acari: Tetranychidae) in Hop

Environmental Entomology ◽

10.1093/ee/nvz071 ◽

2019 ◽

Vol 48 (4) ◽

pp. 894-902 ◽

Cited By ~ 2

Author(s):

A E Iskra ◽

J L Woods ◽

D H Gent

Keyword(s):

Biological Control ◽

Natural Enemies ◽

Nitrogen Fertilization ◽

Spider Mite ◽

Fertilization Rate ◽

Conservation Biological Control ◽

Spider Mites ◽

Economic Damage ◽

Twospotted Spider Mite ◽

Twospotted Spider

Abstract The twospotted spider mite (Tetranychus urticae Koch) is a common pest in agricultural and ornamental crops. This pest can be controlled by resident predatory arthropods in certain situations. This research quantified the stability and resiliency of established conservation biological control of the twospotted spider mite in hop over a 5-yr period associated with nitrogen fertilization rate and use of a broad-spectrum insecticide. Biological control generally was stable and resilient over a sixfold range of nitrogen fertilization rates, and in only 1 of 5 yr did elevated nitrogen rates significantly affect populations of spider mites. In contrast, one application of the insecticide bifenthrin was associated with disruption of biological control and a severe outbreak of spider mites. The complex of natural enemies suppressed the outbreak during the same year in which bifenthrin was applied, but only after populations of spider mites exceeded levels associated with economic damage. However, in the following year the system returned to an equilibrium state where spider mites were suppressed below economically damaging levels. Therefore, conservation biological control in hop appears stable and robust to factors such as nitrogen fertilization that increase reproductive rates of spider mites but may be sensitive to factors such as nonselective insecticides that are lethal to natural enemies. Conservation biological control can be considered resilient to a single use of a nonselective insecticide in the year following the application, but not within the year of application.

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Cytoplasmic-nuclear incompatibility between wild-isolates of Caenorhabditis nouraguensis

10.1101/083154 ◽

2016 ◽

Author(s):

Piero Lamelza ◽

Michael Ailion

Keyword(s):

Genetic Basis ◽

Hybrid Sterility ◽

Reproductive Barrier ◽

Reproductive Barriers ◽

Cytoplasmic Factor ◽

Hybrid Inviability ◽

Hybrid Incompatibility ◽

Endosymbiotic Bacteria ◽

Nuclear Locus ◽

Shed Light

ABSTRACTHow species arise is a fundamental question in biology. Species can be defined as populations of interbreeding individuals that are reproductively isolated from other such populations. Therefore, understanding how reproductive barriers evolve between populations is essential for understanding the process of speciation. Hybrid incompatibility (e.g. hybrid sterility and lethality) is a common and strong reproductive barrier in nature, but few studies have molecularly identified its genetic basis. Here we report a lethal incompatibility between two wild-isolates of the nematode Caenorhabditis nouraguensis. Hybrid inviability results from the incompatibility between a maternally inherited cytoplasmic factor from each strain and a recessive nuclear locus from the other. We have excluded the possibility that maternally inherited endosymbiotic bacteria cause the incompatibility by treating both strains with tetracycline and show that hybrid death is unaffected. Furthermore, cytoplasmic-nuclear incompatibility commonly occurs between other wild-isolates, indicating that this is a significant reproductive barrier within C. nouraguensis. We hypothesize that the maternally inherited cytoplasmic factor is the mitochondrial genome and that mitochondrial dysfunction underlies hybrid death. This system has the potential to shed light on the dynamics of divergent mitochondrial-nuclear coevolution and its role in promoting speciation.

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Revisiting the Hybridization Processes in the Triatoma brasiliensis Complex (Hemiptera, Triatominae): Reproductive Isolation between Triatoma petrocchiae and T. b. brasiliensis and T. lenti

Insects ◽

10.3390/insects12111015 ◽

2021 ◽

Vol 12 (11) ◽

pp. 1015

Author(s):

Luiza Maria Grzyb Delgado ◽

Jader de Oliveira ◽

Amanda Ravazi ◽

Fernanda Fernandez Madeira ◽

Yago Visinho dos Reis ◽

...

Keyword(s):

Reproductive Isolation ◽

The Other ◽

Reproductive Barriers ◽

Prezygotic Isolation ◽

Hatch Rate ◽

Long Time ◽

Experimental Crosses

Triatoma petrocchiae is a species morphologically similar to T. b. brasiliensis (which resulted in a synonymization event); despite this similarity, genetic, morphological, and experimental crossbreeding studies confirmed the specific status of T. petrocchiae. Considering that both species have been reported living in sympatry and that, for a long time, most species of the T. brasiliensis complex were considered only chromatic variants of T. b. brasiliensis, we carried out experimental crosses between T. b. brasiliensis and T. petrocchiae (to confirm whether these species are reproductively isolated) and between T. lenti and T. petrocchiae (to assess whether T. petrocchiae also presents prezygotic isolation with the other species of the T. brasiliensis complex). Reciprocal experimental crosses were conducted, and weekly, the eggs were collected, counted, and separated in new containers to assess the hatch rate. Neither cross resulted in hybrids, demonstrating that there are pre-zygotic reproductive barriers installed between T. petrocchiae and the other species of the T. brasiliensis complex. On the basis of the results above, we demonstrated that T. petrocchiae is reproductively isolated from T. b. brasiliensis and T. lenti. Furthermore, we suggest that T. petrocchiae is the species most derived from the T. brasiliensis complex.

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