Research Article |
Corresponding author: Ilya A. Gavrilov-Zimin ( coccids@gmail.com ) Academic editor: Valentina G. Kuznetsova
© 2024 Ilya A. Gavrilov-Zimin.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Gavrilov-Zimin IA (2024) Gallophilous theory of cyclical parthenogenesis in aphids (Homoptera, Aphidinea). Comparative Cytogenetics 18: 247-276. https://doi.org/10.3897/compcytogen.18.136095
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The paper elaborates theoretical basis of the origin of aphid cyclical parthenogenesis in view of the original life of these insects in strobiloid galls on Picea spp. The period of gall opening is greatly extended in time, which prevents normal panmixia and creates a selective advantage for parthenogenetic reproduction. Migration of aphids to secondary host plants, on which closed galls never form, parthenogenetic reproduction on these plants, and the subsequent simultaneous return of “remigrants” to the main host plant make it possible to synchronize the development of the bisexual generation and achieve mass panmixia at the end of the life cycle only; it coincides with the end of summer growth shoots or the autumn end of the vegetation period as a whole. The evolutionary transition of aphids from conifers to angiosperms in the Cretaceous period in parallel meant the possibility of development in more spacious galls accommodating several consecutive parthenogenetic generations, the transition to viviparity and telescopic embryonization, significantly accelerating the propagation.
Adelgidae, Eriosomatidae, evolution, galls, oviparity, Pemphigidae, Phylloxeridae, unisexual (virgin) reproduction, viviparity
Insects of the suborder Aphidinea (aphids), among all organisms, are characterized by one of the most aberrant reproductive modes, combining both extremely rare and absolutely unique features. An extensive literature is devoted to this topic, but a reader can check the most general modern reviews (
Such alternation is an apomorphic character of the entire suborder Aphidinea and among the approximately 5000 modern species of aphids not a single one is known that does not have parthenogenetic generations. Moreover, all species of aphids known only from parthenogenetic generations are considered to have lost their bisexual generation, usually coincident with loss of the primary host plant (
Menwhile, among Heteroptera (about 50 000 species), in Cicadinea (about 50 000 species) and Psyllinea (about 3,500 species), examples of usual thelytokous parthenogenesis occur as rare exceptions (
In general, for insects and other animals, constant bisexual reproduction is the main, absolutely dominant method of reproduction, the selective advantage of which is undoubtedly due to increased heterozygosity and a corresponding increase in the range of variability in populations. The theoretical basis for the selective advantage of bisexual reproduction has been developed in detail in numerous publications on population genetics and evolutionary theory (see, for example,
The names of higher taxa of aphids and other related insects are given according to the nomenclature-taxonomic system from
Since all modern species of aphids possess parthenogenetic generations in their life cycle, and it is not possible to reliably judge the nature of reproduction of extinct species, the time of transition from obligate bisexuality to heterogony can only be determined very approximately.
The first remnants of aphids are known from the Triassic period (
Hypothetical scheme of the evolution of reproductive peculiarities in aphids. The bold lines designate presumable paraphyletic taxa.
The life of aphids on bark or needles is not fundamentally different from the life of other related groups of insects living on gymnosperms, but do not have cyclic parthenogenesis (for example, coccids, true bugs, cycads). A unique feature that distinguishes adelgids from all these insects is the ability to induce the formation of closed galls, very similar and probably homologous to strobili (Fig.
Mature gall of Adelges sp., Poland. Photo & copyrights: https://www.flickr.com/photos/hedera_baltica/52949379151/.
It is logical to speculate that in the early stages of aphid evolution, when the first adelgids or their ancestors began to live on the ancestors of modern spruce trees, the formation of galls occurred in the same way as now. Reliable paleontological finds attributed to the modern genus Picea Dietrich, 1824 have been known since close to the beginning of the Cretaceous period, 136 million years ago (
Transverse section of gall of Adelges cooleyi (Gillette, 1907) with nymphs inside, USA. Photo & copyrights: Whitney Cranshaw, https://www.insectimages.org/browse/detail.cfm?imgnum=5422255.
In the splitting approach to the taxonomy of adelgids, it is often believed galls that formed in different parts of the crown and open at different times are caused by different “cryptic” species from 7 different genera of adelgids (
It is extremely difficult to understand how most of these “species” differ from each other, since the existing identification keys (for example,
The fate of the third generation of adelgids that settled on the main host plant and on secondary plants turned out to be different. On spruce trees, females of the third generation began feeding on young shoots (as the most favorable place for feeding) and their progeny again found itself locked inside the galls. The change of generations on spruce trees, thus, turned out to be cyclic and exclude bisexual reproduction entirely.
On secondary host plants, sap sucking did not lead to the formation of galls and, accordingly, there were no physical obstacles to the free mating of males and females. However, due to the asynchrony of the two previous generations, the problem remained of re-synchronizing the appearance of males and females in mass numbers and their meeting in the same place, which is necessary for effective cross-fertilization. The only opportunity for such secondary synchronization was the time of approximately the same end of growth of shoots of coniferous trees by the middle of the warm season. In modern conditions, depending on the specific region and the conditions of a particular year, shoot growth ends by the end of June-beginning of July (
Thus, the occurrence of a complicated cyclical change of parthenogenetic and bisexual generations in aphids can be explained by the same basic biological reasons that appeared at the initial stage of the evolution of oogamous multicellular organisms and continue to operate up to now; namely, the problems of mass synchronous production of gametes and their concentration in the same place of space (
Generalized scheme of cyclical parthenogenesis in holocyclic aphids with diploid chromosome number 4 (after
Aphid spermatogenesis occurs in a unique way. Instead of the usual male meiosis producing four identical gametes, aphids produce only two sperm, both with X chromosomes (
Below I shall consider the real life cycles of modern adelgid species, which seem to be rather similar with the hypothetical cycle of their ancestor.
Amongst about 70 recent nominal species of adelgids, combining in the genera Adelges and Pineus, only 24 species are considered as holocyclic (or probably holocyclic): Adelges cooleyi (Gillette, 1907), A. glandulae (Zhang, 1980), A. isedakii Eichhorn, 1978, A. karafutonis Kono et Inouye 1938, A. kitamiensis (Inouye, 1963), A. knucheli (Schneider-Orelli et Schneider, 1954), A. lariciatus (Patch, 1909), A. laricis Vallot, 1836, A. merkeri (Eichhorn, 1957), A. nordmannianae (Eckstein, 1890), A. pectinatae (Cholodkovsky, 1888), A. prelli (Grosmann, 1935) A. roseigallis (Li et Tsai, 1973), A. tardoides (Cholodkovsky, 1911), A. torii (Eichhorn, 1978), A. tsugae Annand, 1924, A. viridis (Ratzeburg, 1843), Pineus armandicola Zhang et al., 1992, P. cembrae (Cholodkovsky, 1888), P. floccus (Patch, 1909), P. orientalis (Dreyfus, 1888), P. pinifoliae (Fitch, 1858), P. sichunanus Zhang, 1980, P. strobi (Hartig, 1839).
The detailed information on all mentioned species can be easily found on the site of R. Blackman and V. Eastop: https://aphidsonworldsplants.info/, and also in the main monographs on Nearctic and Palaearctic species:
The larvae of these holocyclic species form closed galls on the spring shoots of various spruce species (Picea spp.), and during the summer the larvae emerge from the opened galls, molt for the last time and become winged migrants (Fig.
Biennial life cycle of Adelges nordmannianae (Eckstein, 1890) (Aphidinea) (after
The life cycles of most of these species fully correspond to the supposed cycle (described above) of the ancestral species for adelgids and aphids in general. However, several nominal species of the genus Pineus (less archaic than Adelges) show interesting nuances and deviations. Thus, in the American nominal species Pineus strobi (Hartig, 1839) (allegedly widely distributed throughout the Palaearctic), in the USA, the usual migration occurs between primary food plants (Picea spp.) and Weymouth pine (Pinus strobus Linnaeus, 1753) (
The remaining “species” (about 50–55) from the genera Adelges and Pineus were described according to parthenogenetic generations, living on secondary host plants, less often on spruce trees (in galls or cracks in the bark). It is known about many of these “species” that in the summer winged sexuparae appear among the wingless parthenogenetic females, but their further fate has not been traced. In other cases, a detailed examination of the morphology and lifestyle makes it easy to guess from which full-cycle species the corresponding parthenogenetic lineages originate. Thus, unholocyclic A. aenigmaticus Annand, 1928, A. diversis Annand, 1928, A. geniculatus (Ratzeburg, 1844), A. japonicus (Monzen, 1929), A. karamatsu Inouye, 1945, A. lapponicus (Cholodkovsky, 1889), A. oregonensis Annand, 1928, and A. tardus (Dreyfus, 1888), as well as holocyclic A. isedakii Eichhorn, 1978, A. lariciatus (Patch, 1909), and A. tardoides (Cholodkovsky, 1911), in fact are the variations of Adelges laricis Vallot, 1836 – see more detail comments on R. Blackman’s and V. Istop’s site: (https://aphidsonworldsplants.info/d_APHIDS_A/#Adelges).
An interesting feature is known in the gall-inhabiting generation of Pineus similis (Gillett, 1907), which supposedly develops only on spruce trees, without migrating to secondary host plants. Two variants of larvae feed in the galls. Usual larvae give rise to winged migrants that fly to the branches of the same spruce or neighboring spruce trees. Other larvae moult directly inside the gall onto wingless females, which lay eggs there (
The second group of aphids characterized by obligate oviposition in all generations is the family Phylloxeridae — phylloxeras. The cyclic parthenogenesis of these aphids, combined with the loss of the ovipositor and the complete absence of connections with gymnosperms, allows to say that phylloxeras are not just a sister group to adelgids (as is often indicated in aphidological literature, e.g.
Gall of Phylloxera sp. on leaf of hickory, USA. Photo & copyrights: Judy Gallagher, https://www.flickr.com/photos/52450054@N04/50955746943/.
Gall of Phylloxera sp. on leaf of hickory, USA. Photo & copyrights: Katja Schulz, https://www.flickr.com/photos/treegrow/48516072207/.
In the Palearctic fauna, the diversity of phylloxeras is in all respects significantly lower than in the Nearctic. Firstly, among the Palaearctic species, not a single one is known to migrate to unrelated host plants. Only for Phylloxera quercus Boyer de Fonscolombe, 1834 in the Mediterranean is migration between different (evergreen and deciduous) oak species known. Secondly, with the exception of Olegia ulmifoliae (Aoki, 1973), which lives in closed galls on elm leaves, there are no gall-forming phylloxeras in the Palearctic. Thirdly, the range of food plants of Palaearctic phylloxeras is limited mainly to oaks, willows and poplars. One species is also known from elm, pear and chestnut. All three of these species are represented exclusively by wingless generations, as are the species living on willows and poplars. Among Palearctic species that feed on oaks, winged females are known only for a few species from the type genus Phylloxera Boyer de Fonscolombe, 1834 (
Thus, analysis of food connections and life cycles allows to conclude that the origin of phylloxeras as a taxonomic group was connected with hickories in North America. Probably, the evolutionary transition from gymnosperms, on which the adelgid ancestor of phylloxeras lived, to hickory was due to the fact that, of the Nearctic angiosperms common in the Cretaceous period, only hickory formed galls and this allowed the first phylloxeras to develop in the usual cycle of alternation of gall and freeliving generations. It is believed that Carya spp. appeared in North America in the second half of the Cretaceous period, and related extinct plant genera even earlier (
The proposed transition from living in closed galls on spruce trees to living in closed galls on hickory leaves, petioles or shoots would inevitably lead to changes in the reproductive biology of the first phylloxera. 1) Unlike the cramped internal cavities of spruce galls, hickory galls, as they grow, form a large space that far exceeds the body volume of an adult aphid. This circumstance allowed the first generation of the inhabitants of the galls not to wait for their opening, but to lay eggs just inside the gall, with the subsequent development of the second and even third generations there. In some modern species, the productivity of gall inhabitants turns out to be extremely high: in Phylloxera devastatrix Pergande, 1904 — from 300 to 1300 individuals per gall, depending on its size (
On the other hand, all these changes do not cancel other circumstances that played an important role in the evolution of adelgids and remained factors in the evolution of more advanced groups of aphids. These circumstances are the impossibility of synchronization and mass cross-fertilization during development in closed galls and a sharp decrease in the nutritional value of tree shoots by the middle of the warm period of the year. The action of these factors, combined with the possibility of the development of several gall generations on hickory, led to a significantly greater diversity of phylloxeras life cycles and host connections compared to adelgids. Some phylloxera species have maintained regular migrations from hickories to secondary host plants (oaks, chestnuts, and possibly some others). Other phylloxeras have switched to permanent holocyclic development on hickory. The third groups of species began to develop exclusively on secondary host plants, forming certain leaf deformations on them or forming open galls that do not interfere with the free synchronous emergence of sexuparae and/or bisexual generations. A fourth group of species, probably due to the gradual evolution of the chemistry of their saliva, began to form open galls on the hickories themselves. On the other hand, the formation of closed or open galls on hickory apparently depended not only on the evolution of phylloxeras, but also on the gradual physiological and morphological evolution of different species of these trees. It cannot be ruled out that at the very beginning of the evolution of phylloxeras, females of their common ancestor had already formed both closed and open galls, depending on what type of hickory and on what part of it (leaf blade, petiole or base of a young shoot) they started to feed. In any case, the obvious multidirectionality of the reproductive evolution of phylloxeras and the sharp expansion of their host connections in comparison with adelgids allows us to speak of their significant similarity in these parameters with Aphidoidea aphids. At the same time, neither phylloxeras nor Aphidoidea can return to constant bisexual reproduction, which was in the ancestors of aphids, due to the developed specific features of gametogenesis and the exclusively parthenogenetic method of formation of the bisexual generation (see above). Their life cycle must include at least one parthenogenetic generation, alternating with a bisexual one. Such a reproductive “minimum” is actually achieved in some modern species, for example, in the European oak phylloxera Acanthochermes quercus Kollar, 1848 (Fig.
Larvae of fundatcises of Acanthochermes quercus Kollar, 1848 on oak leaf, Abkhazia. Photo of A.S. Kurochkin.
It is also necessary to note two interesting ontogenetic features of phylloxeras, the evolutionary significance and prevalence of which remain poorly understood. Firstly, according to the observation of M.
All modern species of aphidoid aphids are characterized by the loss of the ovipositor. Taking into account this fact, reproductive characteristics and the nature of host connections, it is logical to believe that aphidoid aphids originated in the Cretaceous from a certain ancient species of phylloxeras. Otherwise, we would have to admit that the complex of characters (cyclical parthenogenesis, a unique cytogenetic system, loss of the ovipositor, the transition from gymnosperms to angiosperms) arose independently several times in the evolution of aphids; the first time in the adelgid-phylloxera branch for the reasons discussed above, and at least twice in aphidoid aphids for some other unknown reasons. Such an extraordinary combination of a number of evolutionary coincidences seems absolutely incredible. All the few connections between aphidoid aphids and gymnosperms are clearly of a secondary nature. Such connections are found in a number of genera of lachnids (Lachnidae), in representatives of the genus Neophyllaphis Takahashi, 1920 (Drepanosiphidae) and in some genera of eriosomatids (Eriosomatidae). These examples require somewhat more detailed consideration.
Lyachnids of the subfamily Cinarinae, widespread in the Holarctic and associated with various species of pines (Pinus spp.), spruce (Picea spp.), fir (Abies spp.), larch (Larix spp.), and cypress (Cupressaceae), are considered either by different aphidologists as one of the youngest, most advanced groups of aphidoid aphids, or, conversely, as one of the most archaic (see review of competing opinions in
Aphids of the genus Neophyllaphis of the monotypic subfamily Neophyllaphidinae are represented in the modern fauna by 18 species associated with gymnosperms of the families Podocarpaceae and Araucariaceae, mainly in the Southern Hemisphere, including in the mountainous regions of the tropical zone of the planet. All these species develop unholocyclically, but in a number of cases they demonstrate holocycly, with the appearance of winged (rarely wingless) individuals of the bisexual generation (Blackman & Eastop, https://aphidsonworldsplants.info/d_APHIDS_N/#Neophyllaphis). The very fact that these aphids, like their host plants, in their distribution are separated from the obvious center of diversity and origin of aphids, i.e. from the temperate climate zone of the Holarctic, does not in itself allow us to consider them an ancestral group in relation to other aphidoid aphids. For one of the species, N. brimblecombei Carver, 1971, a feeding relationship with eucalyptus (Eucalyptus robusta Smith, 1792) was indicated in southern China, where the species was apparently introduced from Australia (
Phylogenetic reconstructions proposed by various authors for other groups of aphidoid aphids are extremely contradictory (
The family Eriosomatidae is divided into three subfamilies: Eriosomatinae, Fordinae and Pemphiginae. Aphids of Eriosomatinae (genera Aphidounguis Takahashi, 1963, Byrsocryptoides Dzhibladze, 1960, Colopha Monell, 1877, Colophina Börner, 1931, Eriosoma Leach, 1818, Gharesia Stroyan, 1963, Hemipodaphis David et al., 1972, Schouteden, 1906, Paracolopha Hille Ris Lambers, 1966, Schizoneurata Hille Ris Lambers, 1973, Schizoneurella Hille Ris Lambers, 1973, Siciunguis Zhang et Qiao, 1999, Tetraneura Hartig, 1841, Zelkovaphis Barbagallo, 2002) mainly use as their primarily host plants various Ulmus spp. and Zelkova spp., on the leaves of which they form closed or open galls (Fig.
Galls of Tetraneura ulmi (Linnaeus, 1758) on elm leaf, USA. Photo & copyrights: Judy Gallagher, https://www.flickr.com/photos/52450054@N04/33994074962/.
For the subfamily Fordinae (genera Aloephagus Essig, 1950, Aploneura Passerini, 1863, Asiphonella Theobald, 1923, Baizongia Rondani, 1848, Chaetogeoica Remaudière et Tao, 1957, Dimelaphis Zhang, 1998, Floraphis Tsai et Tang, 1946, Forda von Heyden, 1837, Geoica Hart, 1894, Geopemphigus Hille Ris Lambers, 1933, Inbaria Barjadze et al., 2018, Kaburagia Takagi, 1937, Meitanaphis Tsai et Tang, 1946, Melaphis Walsh, 1867, Nurudea Matsumura, 1917, Paracletus von Heyden, 1837, Qiao Hébert et al., 2022, Rectinasus Theobald, 1914, Schlechtendalia Lichtenstein, 1883, Slavum Mordvilko, 1927, Smynthurodes Westwood, 1849, Tramaforda Manheim, 2007) the primarily host plants are Pistacia spp. and Rhus spp. Closed or open galls are formed on the leaves of these plants (Fig.
Galls of two different species of Fordinae on twigs of Pistacia terebinthus Linnaeus, 1753. Photo & copyrights: Gene Selkov, https://www.flickr.com/photos/selkovjr/45002126051/.
The aphids of the subfamily Pemphiginae (genera Ceratopemphigiella Menon et Pawar, 1958, Ceratopemphigus Schouteden, 1905, Clydesmithia Danielsson, 1989, Cornaphis Gillette, 1913, Diprociphilus Zhang et Qiao, 1999, Epipemphigus Hille Ris Lambers, 1966, Formosaphis Takahashi, 1925, Furvaphis Hong, 2002, Gootiella Tullgren, 1925, Grylloprociphilus Smith et Pepper, 1968, Mimeuria Börner, 1952, Mordwilkoja Del Guercio, 1909, Neopemphigus Mamontova et Kolomoets, 1981, Neoprociphilus Patch, 1912, Pachypappa Koch, 1856, Pachypappella Baker, 1920, Patchiella Tullgren, 1925, Pemphigus Hartig, 1839, Prociphilus Koch, 1857, Thecabius Koch, 1857, Tiliphagus Smith, 1965, Uichancoella Calilung, 1975) use mainly Populus spp. as primarily host plants, but sometimes inhabit also the other arboral angiosmerms. Spring generations feed inside closed or open galls on the leaves or petioles of poplar leaves, and winged migrants, emerging from the galls, usually fly to the roots of coniferous trees, less often to herbaceous angiosperms. The genus Prociphilus differs from other genera of the subfamily in an unusually wide range of primary host plants (from the families Rosaceae, Caprifoliaceae, Oleaceae, etc.), but summer migration is still carried out to the roots of coniferous trees. Some species, for example, Pemphigus spyrothecae Passerini, 1860, which lives in closed galls on poplars (Fig.
Galls of Pemphigus spyrothecae Passerini, 1860 on petioles of poplar, Samara Prov. of Russia. Photo of A.S. Kurochkin.
Thus, in all three subfamilies of Eriosomatidae, many species demonstrate an archaic life cycle, characteristic of adelgids, with development inside closed galls. In the subfamily Fordinae a number of species even demonstrate a two-year cycle, again characteristic of adelgids. This fact further illustrates the extreme dependence of the aphid life cycle on the specific gall formation on specific plants. It is impossible to imagine that such a prolongation of the cycle would be evolutionarily beneficial for the corresponding aphid species, in any way “controlling” the development of the gall. However, it is quite logical to explain this situation by the simple impossibility of leaving the closed galls before the end of the summer season. The appearance of placental viviparity and telescopic embryonization, which occurred for the first time probably among eriosomatids, makes it possible to significantly accelerate the change of generations, and, consequently, increase the number of descendants, regardless of the time of gall opening. Of course, this is only possible if there is sufficient internal space in the gall, which also depends on the exact host plant peculiarities.
Among other aphidoid aphids, life in closed galls is known only for a number of genera/species of Hormaphididae, assigned to the tribe Cerataphidini (
In aphidoid aphids of the families Aphididae, Drepanosiphidae, Mindaridae, some species form different “pseudogalls”, which are curled leaves or needles of host plants. Such shelters do not pose problems for the free exit of migrating winged individuals of aphids, and this exit occurs as the growth of the shoots of the corresponding plants ends and their nutritional value decreases (
From the above consideration of the life cycles and reproductive peculiarities of aphids, it is clear that the evolution of their archaic groups: adelgids, phylloxeras, eriosomatids, and hormaphidids is fully or partially associated with life in closed galls formed on gymnosperms or angiosperms. Living in closed galls fundamentally distinguishes these aphids from other related groups of hemipteroid gall-forming insects: scale-insects, psyllids and some true bugs; among these groups, there are no examples of the formation of closed galls nor examples of cyclical parthenogenesis, although other (non-cyclical) variants of parthenogenesis are quite common (especially in scale-insects) (
In this article, it is not possible or necessary to consider the remaining numerous groups of gall-forming animals, but it can be noted that among terrestrial animals, regular cyclical parthenogenesis has been proven only for some gall wasps (Hymenoptera: Cynipidae) living in closed galls (
More or less regular heterogony is also known in a number of groups of primary aquatic animals, for example, in some trematodes, rotifers and crustaceans (
The frequent reference in the review literature (see, for example,
Just as often and erroneously, the life cycle of the beetle Micromalthus debilis LeConte, 1878 is cited as an example of cyclical parthenogenesis. However, the reproduction of this species is carried out exclusively by parthenogenesis (
Summarizing the results of the discussion, we can highlight the following main theses characterizing the evolution of the reproductive characteristics of aphids.
I am very grateful to Prof. V.G. Kuznetsova and anonymous reviewers for important remarks, to A.S. Kurochkin and foreign specialists (Whitney Cranshaw, Judy Gallagher, Katja Schulz, Gene Selkov), including anonymous ones, whose photographs are used in this article under a Creative Commons license. The work was carried out within the framework of the state assignment of the Zoological Institute of the Russian Academy of Sciences No. 122031100272-3.
Ilya A. Gavrilov-Zimin https://orcid.org/0000-0003-1993-5984