Rare diploid females coexist with rare males: a novel finding in triploid parthenogenetic populations in the psyllid Cacopsylla myrtilli (W. Wagner, 1947) (Hemiptera, Psylloidea) in northern Europe
Abstract:Using a cytological approach, diploid females were found coexisting with rare males in triploid apomictic parthenogenetic populations of the psyllid Cacopsylla myrtilli (W. Wagner, 1947) in Norway, Sweden, Finland and northwest Russia. Diploid females were easily distinguished from triploid apomictic females by the presence of 13 chiasmate bivalents instead of 39 univalent chromosomes at metaphase I. Abundance equaled that of males, but the proportion of males and diploid females was significantly greater in h… Show more
“…Our findings show that details of parthenogenesis in C.ledi are similar to those found previously in C.myrtilli (Nokkala et al 2015). Parthenogenetic females of C.ledi are triploid showing apomictic oogenesis in which normal meiosis is replaced by a modified mitosis.…”
Section: Discussionsupporting
confidence: 90%
“…In addition to triploid females, there were also diploids showing normal chiasmate meiosis. Moreover, the presence of diploid females among obligate triploid parthenogenetic females was discovered for the first time in populations of C.myrtilli collected at various altitudes on the hill Rindhovda in southern Norway (Nokkala et al 2015). Diploid females showing conventional meiosis were found at frequencies similar to those of rare males at three different altitudes.…”
Section: Discussionmentioning
confidence: 98%
“…A fragment of cytochrome c oxidase subunit I ( COI ) gene was amplified using Applied Biosystems 2720 Thermal Cycler. Initially, the C.myrtilli specific primers HybCamyCO (forward) and HybymaCCO (reverse) were used and PCR reactions were carried out as described by Nokkala et al (2015). Later on, to check the sequence at 5’ and 3’ ends, flanking primers HybCacoCO 5’-T7Promoter(F)-CTAACCATAARACTATTGGAAC-3’ (specifically designed forward primer) and a modified HCO (Folmer et al 1994) reverse primer HybHCOMod 5’-T3-TAAACTTCAGGGTGACAAAAAATCA-3’ were used.…”
Section: Methodsmentioning
confidence: 99%
“…PCR products were purified with QIAquick PCR Purfication Kit (Qiagen) and sequenced by Macrogen Europe (Amsterdam, the Netherlands). The sequences were trimmed to span a 638 bp stretch of the gene to match the available sequences of related C.myrtilli (Nokkala et al 2015). Sequences obtained during this study have been deposited in GenBank under the accession numbers MF978762-MF978766.…”
Section: Methodsmentioning
confidence: 99%
“…Cytological analysis has also discovered diploid females coexisting with the rare males especially at high altitude. These rare males, although being nonfunctional, copulate randomly with both parthenogenetic and “sexual” diploid females (Nokkala et al 2015). …”
Characteristics of parthenogenesis in Cacopsylla
ledi (Flor, 1861) were analyzed using cytological and molecular approaches. In all three populations studied from Finland, i.e. Turku, Kustavi and Siikajoki, males were present at a low frequency but were absent from a population from Vorkuta, Russia. In a follow-up study conducted in the Turku population during 2010–2016, the initial frequency of males was ca. 10 % and showed no intraseasonal variation, but then dramatically decreased down to approximately 1–2 % level in seasons 2015–2016. Male meiosis was chiasmate with some traces of chromosomal fragmentation and subsequent fusions. In most females, metaphase in mature eggs included 39 univalent chromosomes which indicated apomictic triploidy. Only a small fraction of females was diploid with 13 chiasmate bivalents. The frequency of diploid females approximately equaled that of males. COI barcode analyses showed that triploid females (N = 57) and diploids (7 females and 5 males) displayed different haplotypes, demonstrating that triploid females reproduced via obligate parthenogenesis. The rarity of diploids, along with the lack of males’ preference towards diploid females, suggested that most likely diploids were produced by rare triploid females which shared the same haplotype with the diploids (not found in the present analysis). Minimum haplotype diversity was detected in the Turku population, but it was much higher in Vorkuta with some indication for the mixed origin of the population. We suggest that functional diploids produced in a parthenogenetic population can give rise either to a new parthenogenetic lineage or even to a new bisexual species.
“…Our findings show that details of parthenogenesis in C.ledi are similar to those found previously in C.myrtilli (Nokkala et al 2015). Parthenogenetic females of C.ledi are triploid showing apomictic oogenesis in which normal meiosis is replaced by a modified mitosis.…”
Section: Discussionsupporting
confidence: 90%
“…In addition to triploid females, there were also diploids showing normal chiasmate meiosis. Moreover, the presence of diploid females among obligate triploid parthenogenetic females was discovered for the first time in populations of C.myrtilli collected at various altitudes on the hill Rindhovda in southern Norway (Nokkala et al 2015). Diploid females showing conventional meiosis were found at frequencies similar to those of rare males at three different altitudes.…”
Section: Discussionmentioning
confidence: 98%
“…A fragment of cytochrome c oxidase subunit I ( COI ) gene was amplified using Applied Biosystems 2720 Thermal Cycler. Initially, the C.myrtilli specific primers HybCamyCO (forward) and HybymaCCO (reverse) were used and PCR reactions were carried out as described by Nokkala et al (2015). Later on, to check the sequence at 5’ and 3’ ends, flanking primers HybCacoCO 5’-T7Promoter(F)-CTAACCATAARACTATTGGAAC-3’ (specifically designed forward primer) and a modified HCO (Folmer et al 1994) reverse primer HybHCOMod 5’-T3-TAAACTTCAGGGTGACAAAAAATCA-3’ were used.…”
Section: Methodsmentioning
confidence: 99%
“…PCR products were purified with QIAquick PCR Purfication Kit (Qiagen) and sequenced by Macrogen Europe (Amsterdam, the Netherlands). The sequences were trimmed to span a 638 bp stretch of the gene to match the available sequences of related C.myrtilli (Nokkala et al 2015). Sequences obtained during this study have been deposited in GenBank under the accession numbers MF978762-MF978766.…”
Section: Methodsmentioning
confidence: 99%
“…Cytological analysis has also discovered diploid females coexisting with the rare males especially at high altitude. These rare males, although being nonfunctional, copulate randomly with both parthenogenetic and “sexual” diploid females (Nokkala et al 2015). …”
Characteristics of parthenogenesis in Cacopsylla
ledi (Flor, 1861) were analyzed using cytological and molecular approaches. In all three populations studied from Finland, i.e. Turku, Kustavi and Siikajoki, males were present at a low frequency but were absent from a population from Vorkuta, Russia. In a follow-up study conducted in the Turku population during 2010–2016, the initial frequency of males was ca. 10 % and showed no intraseasonal variation, but then dramatically decreased down to approximately 1–2 % level in seasons 2015–2016. Male meiosis was chiasmate with some traces of chromosomal fragmentation and subsequent fusions. In most females, metaphase in mature eggs included 39 univalent chromosomes which indicated apomictic triploidy. Only a small fraction of females was diploid with 13 chiasmate bivalents. The frequency of diploid females approximately equaled that of males. COI barcode analyses showed that triploid females (N = 57) and diploids (7 females and 5 males) displayed different haplotypes, demonstrating that triploid females reproduced via obligate parthenogenesis. The rarity of diploids, along with the lack of males’ preference towards diploid females, suggested that most likely diploids were produced by rare triploid females which shared the same haplotype with the diploids (not found in the present analysis). Minimum haplotype diversity was detected in the Turku population, but it was much higher in Vorkuta with some indication for the mixed origin of the population. We suggest that functional diploids produced in a parthenogenetic population can give rise either to a new parthenogenetic lineage or even to a new bisexual species.
In hexapods, unlike the majority of animals, development without fertilization is a common phenomenon. They evolved a striking diversity of unisexual reproductive types that include a variety of modes starting from spontaneous parthenogenesis in females to the production of impaternate males with different variants in between. Many reports about parthenogenetic species have accumulated over time. Here, we present a review of various parthenogenetic hexapod groups with a particular focus on their chromosome systems and ploidy level. We show that conclusions about the reproductive mode often lack solid evidence and sometimes inefficiently demonstrate how parthenogenesis is maintained in corresponding groups. In this review, basal hexapods (Protura, Collembola, Diplura), primarily wingless insect groups (‘Apterygota’) and non‐holometabolous insects are listed with references to a variety of their unisexual reproductive modes.
To reveal the phylogeographic pattern of the parthenogenetic psyllid Cacopsylla myrtilli (W. Wagner 1947) (Hemiptera, Psylloidea), we sequenced a 638 bp fragment of the mitochondrial COI gene from 962 individuals. These insects originated from 46 sampling sites, which cover a significant part of the northern Palearctic distribution range of the species. The sequence data revealed 40 haplotypes, with three main (H1, H2, and H3) and 37 derived ones. The main haplotypes H1 or H2 or both were present at all sampling sites. The star-like shape of the haplotype networks indicated recent population expansion. In most cases, the derived haplotypes were specific for each country, suggesting that the main haplotypes H1 and H2 are of refugial origin, and the derived haplotypes have emerged after the postglacial recolonization process. Based on the haplotype sequences, we suggest H3 to represent the ancestral haplotype from which H1 and H2 have evolved. We suggest that the main haplotype H3 together with its derived haplotypes represents bisexual C. myrtilli, which shows a limited distribution on both sides of the border between Finland and Russia in northern Fennoscandia. The genetic diversity was the highest in Sjoa in southern Norway and also high in the White Sea region in northwest Russia. Higher diversity in Sjoa was attributed to both earlier recolonizations compared to that of the White Sea region and the absence of Wolbachia infection. We suggest that these sites were colonized from different Pleistocene refugia, i.e., from western and eastern refugia, respectively. From the White Sea region, recolonization continued eastwards to Ural Mountains and westwards to Finland and further north to Kola Peninsula. From northern Finland, recolonization continued to Finnmark, Norway, and further to Sweden and finally reached a secondary contact zone with colonizers from Norway in Central Sweden. The Caucasus and Siberian/Manchurian refugial regions have played an important role in the origin of C. myrtilli populations in Siberia and the Russian Far East.
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