Across the data assembled by the researchers, diploid chromosome numbers extended from 2n=4 to approximately 2n=192, with the upper extreme documented in a scale insect and the lower extreme occurring in several unrelated lineages. The central feature of most Paraneoptera is the absence of a single localized centromere. In a conventional monocentric chromosome, centromeric DNA is concentrated in a primary constriction, where kinetochore proteins assemble and connect the chromosome to spindle microtubules during cell division.

A holokinetic chromosome instead has centromeric activity distributed along its whole or nearly whole length, allowing spindle fibers to attach along the chromosome as it moves toward the pole during anaphase. The term “holocentric” is often used, but the review argues that it describes the condition imperfectly because a holokinetic chromosome lacks the defined primary constriction characteristic of a monocentric chromosome and maintains a regular distance between sister chromatids at metaphase. Thrips are the notable exception within Paraneoptera: all studied representatives of both suborders, Terebrantia and Tubulifera, have monocentric rather than holokinetic chromosomes.

Holokinetic organization has major consequences for chromosome mechanics. Fragments produced by chromosome breakage can retain centromeric activity and segregate during cell division, and experiments with irradiated mealybugs and Mediterranean flour moths showed that some fragments can be inherited through somatic tissues, germ cells and, in the moth example, more than 50 generations. Such fragments can also acquire functional telomeres, making it possible for fusions and fissions to persist and spread.

The structure nevertheless has biological constraints: holokinetic bivalents generally have only one or two chiasmata, a feature discussed as a possible evolutionary disadvantage, while the potential advantages of holokinetic organization for exploiting habitats and tolerating stress remain hypotheses. The ability to tolerate rearrangement is therefore a permissive condition, not a guaranteed evolutionary accelerator. The review also places the origin of holokinetic chromosomes in the context of centromere biology.

Independent transitions to this state in insects have repeatedly been associated with loss of the centromeric histone H3 variant, CenH3, a protein central to centromere formation in most eukaryotes. Evidence reviewed by the authors suggests that the holokinetic state probably preceded complete CenH3 loss: some insects with holokinetic chromosomes retain CenH3 homologues, potentially representing intermediate stages. Holokinetic chromosomes are also known across every major lineage of winged insects, suggesting at least four independent origins.

This convergent history matters because it demonstrates that the same chromosome architecture can arise in separate branches rather than defining one inherited state for all insects. The comparison spans every major Paraneoptera lineage, but the quantity of cytogenetic information varies sharply. In bark lice, 90 of 5,941 described species have been studied cytogenetically.

An X(0) sex-determination system is characteristic of nearly all examined species, and a karyotype of 2n=16 autosomes plus XX in females or a single X in males occurs in about 90% of the species for which data are available. Two species have neo-XY systems attributed to X-autosome fusions, while three triploid parthenogenetic species carry 2n=3x=27. True lice are even less thoroughly sampled: only 13 species have chromosome data, yet seven distinct counts from 2n=4 to 2n=24 are already known, and sex chromosomes have not been distinguished in any of them.

Such gaps prevent firm conclusions about ancestral chromosome numbers or modes for several orders. Thrips provide the clearest exception to the holokinetic pattern and show why a broad lineage-level label can conceal major biological variation. Chromosome information is available for only 17 of roughly 5,900 described species, but male haploid numbers range from 10 to approximately 50–53, equivalent to diploid totals of 20 and 100–106.

Two cytotypes of Gynaikothrips uzeli have n=13 and n=15. No sex chromosomes have been detected, and the authors state that the mechanism of sex determination remains unresolved, although a single-locus system is considered plausible. Most studied thrips reproduce by arrhenotoky, with haploid males developing from unfertilized eggs and diploid females from fertilized eggs; thelytokous and, in one species, deuterotokous reproduction have also been documented.

The largest chromosome-number ranges occur among scale insects and aphids, both members of the broader sternorrhynch assemblage and both characterized by diverse reproductive modes. Chromosome counts are known for 506 scale-insect species, about 6% of those described, with 2n=4 in several species and approximately 2n=192 in Apiomorpha macqueeni. The Australian felt-scale genus Apiomorpha alone contains 42 reported diploid counts across 47 studied species, spanning 2n=4 to approximately 192, a 48-fold range accompanied by variation within some named species.

Scale insects also include XX/X(0), multiple-X, paternal genome heterochromatinization and paternal genome elimination systems, although conventional XY has not been confirmed. In aphids, 1,113 species have chromosome counts; the genus Amphorophora spans 2n=4 to 2n=72 across ten observed counts. Most aphids nevertheless have a stable complement, commonly 2n=8, 10 or 12, and their cyclical parthenogenesis involves elimination of specific X chromosomes during oogenesis.

Other sap-feeding lineages show a mixture of stability, local polymorphism and derived sex-chromosome arrangements. Only four whitefly species have been studied cytologically. In Bemisia tabaci, eggs from unmated females had 10 chromosomes, while eggs from mated females had either 10 or 20, indicating a reproductive system more complex than simple haplodiploidy and supporting paternal genome elimination.

In psyllids, about 220 of nearly 4,000 species have been examined, and a male karyotype of 2n=24 autosomes plus an X occurs in approximately 80% of studied species. Some populations carry neo-XY or neo-X1X2Y systems produced by fusions, while B chromosomes, triploid parthenogenesis and pentaploidy have also been documented. Across approximately 850 studied true-hopper species, female chromosome numbers generally range from 8 to 38, but most lie between 20 and 28; counts above 38 are associated with parthenogenesis and polyploidy.

True bugs provide the largest cytogenetic dataset within Paraneoptera, with chromosome information for roughly 1,900 of more than 42,000 described species, or about 5%. Their diploid numbers range from 2n=4 to 2n=80, although most fall between 12 and 34, and a male total of 14 is the most common. XX/XY predominates in the available sample, but XX/X(0), multiple sex-chromosome systems and neo-sex chromosomes also occur.

The human bed bug illustrates extreme X fragmentation, with European populations carrying as many as 20 X chromosomes in some males. True bugs also have distinctive small “m-chromosomes” whose evolutionary function remains uncertain. By contrast, the 36 species of moss bugs are represented by only two studied species, both with holokinetic chromosomes and the sex-chromosome post-reduction behavior characteristic of true bugs, a similarity that supports their close evolutionary relationship.

Together, the assembled evidence supports a qualified conclusion: holokinetic chromosomes have a well-established capacity to undergo fissions, fusions and stable fragment inheritance, but those changes only occasionally become major drivers of karyotype evolution within Paraneoptera. The comparison is consistent with a broader analysis of 4,393 insect species that found no significant difference in chromosome-number evolution between holokinetic and monocentric taxa. Reproductive mode, polyploidy, population structure, meiotic drive and other biological variables may matter more than centromere architecture alone.

The comparison is not definitive because sampling remains uneven and population-level data are scarce, but the review shows why the capacity to tolerate chromosome rearrangement should not be confused with a consistently elevated rate of evolutionary change. For most Paraneoptera lineages, the striking feature is not ceaseless chromosomal churn but the preservation of recognizable ancestral karyotypes within a diversity of sex-determination and reproductive systems.

Subject of Research: Comparative cytogenetics of chromosome numbers and sex-chromosome systems in Paraneoptera insects

Article Title: Comparative analysis of chromosome numbers and sex chromosome systems in Paraneoptera ( Insecta )

Article References: Kuznetsova, V. G., Gavrilov-Zimin, I. A., Grozeva, S. M., & Golub, N. V. (2021). Comparative analysis of chromosome numbers and sex chromosome systems in Paraneoptera (Insecta). Comparative Cytogenetics, 15(3), 279-327. https://doi.org/10.3897/compcytogen.v15.i3.71866

Image Credits: AI Generated

DOI: 10.3897/CompCytogen.v15.i3.71866

Keywords: Paraneoptera, holokinetic chromosomes, chromosome evolution, sex determination, karyotype variation, insect cytogenetics, centromere biology, chromosome fusions, chromosome fissions, parthenogenesis, Comparative, analysis