Mediterranean species of the spittlebug genus Philaenus: modes of chromosome evolution

Abstract

The evolution of karyotypes and sex determination system of Philaenus Stål (Auchenorrhyncha: Aphrophoridae) species is studied here in detail. The most plausible scenario of chromosomal rearrangements accompanying phylogenetic differentiation in Philaenus is advanced. It is postulated that the ancestral karyotype of Philaenus was 2n = 24 + X0. Karyotype changes occurred several times independently in the genus. The karyotype of 2n = 22 + X0 (P. spumarius and P. tesselatus) originated from 2n = 24 + X0 by fusion between two autosomal pairs. The neo-XY system (P. arslani, P. loukasi, P. signatus, P. maghresignus, and P. tarifa) also originated from the 24 + X0 karyotype by means of independent fusions between autosomes and the original X chromosome. The neo-X(1)X(2)Y system (P. italosignus) evolved from the 2n = 22 + neo-XY karyotype by an additional fusion between the Y chromosome and one more autosomal pair. The neo-X(n)Y system of P. italosignus is the first reported case of an evolutionarily fixed multiple sex chromosome system in Auchenorrhyncha.

Figure 1a–g.

Mitotic and meiotic chromosomes of Philaenus tesselatus. (a) mitotic prometaphase; (b) karyogram of mitotic prometaphase; (c) C—banded diakinesis (asterisks indicate two chiasmata in the largest bivalent); (d) C—banded metaphase l; (e) Ag—stained diplotene (arrows indicate NORs); (f) incomplete mitotic prometaphase with NORs—bearing chromosomes (arrows); (g) CMA₃treated metaphase 1 with one positive signal on the largest bivalent (asterisk). Bar = 10 µm. Scale bar on (a) refers to (a), (b), and (f); scale bar on (c) refers to (c), (d), and (e). High quality figures are available online.

Figure 2a–f.

Mitotic and meiotic chromosomes of Philaenus loukasi. (a) mitotic metaphase; (b) karyogram of mitotic metaphase; (c) Ag—stained mitotic metaphase (arrows indicate two clusters of argyrophilic material); (d) diakinesis; (e) C—banded diakinesis, in the larger autosomal bivalent two terminal chiasmata are visible; in small frame the largest autosomal bivalent with terminal and interstitial chiasmata from another plate is added; (f) diplotene, bivalent with three chiasmata (asterisks). Bar = 10 µm. Scale bar on (a) refers to (a) and (b); scale bar on (e) refers to (d), (e), and (f). High quality figures are available online.

Figure 3a–h.

Mitotic and meiotic chromosomes of Philaenus signatus. (a) mitotic metaphase; (b) karyogram of mitotic metaphase; (c) C—banded mitotic prometaphase; (d) interphase, note the neo—X chromosome as a long heteropycnotic body; (e) diakinesis, bivalents are connected by terminal or interstitial chiasmata, asterik indicate two chiasmata in the largest bivalent; (f) C—banded diakinesis; (g) metaphase I; (h) silver—stained mitotic prometaphase (arrows indicate four clusters of argyrophilic material connected to chromosomes other than sex chromosomes). Bar = 10 µm. Scale bar on (c) refers to (a), (b), and (c); scale bar on (e) refers to (d–h). High quality figures are available online.

Figure 4a–e.

Mitotic and meiotic chromosomes of Philaenus tarifa. (a) mitotic metaphase; (b) karyogram of mitotic metaphase; (c) diakinesis, bivalents with one or two chiasmata, asterisks indicate two chiasmata in a large bivalent; (d) C—banded diakinesis; (e) Ag—stained diplotene, arrows indicate two bivalents bearing NORs. Bar = 10 µm. Scale bar on (a) refers to (a) and (b); scale bar on (c) refers to (c), (d), and (e). High quality figures are available online.

Figure 5a–d.

Mitotic and meiotic chromosomes of Philaenus maghresignus. (a) mitotic metaphase; (b) karyogram of mitotic metaphase; (c) C—banded diplotene; (d) C—banded diakinesis, one telomere of the neo—X is marked with a large block of heterochromatin (arrow), asterisks indicate two chiasmata in large autosomal bivalents. Bar = 10 µm. Scale bar on (a) refers to (a) and (b); scale bar on (c) refers to (c) and (d). High quality figures are available online.

Figure 6a–1.

Mitotic and meiotic chromosomes of Philaenus italosignus. (a) mitotic metaphase; (b) karyogram of mitotic metaphase; (c) C—banded mitotic prometaphase; (d) C—banded karyogram of mitotic prometaphase; (e) and (f) C—banded diplotene/diakinesis, sex trivalent with chromosomes joint end— to—end in order: X₁-Y-X₂; (g) C—banded diakinesis, sex chromosomes appear as univalents (outlined); (h) Ag—stained diplotene, asterisk indicates three chiasmata in one bivalent; headarrow indicates NOR; (i) two daughter metaphases II with n = 10 + X₁X₂ and n = 10 + Y, respectively; (j) and (k) Ag—stained mitotic prometaphases with four and two NORs, respectively (arrows); (I) CMA₃—treated metaphase I with one positive signal on the sex—chromosome trivalent (asterisk). Bar = 10 µm. Scale bar on (d) refers to (a–d); scale bar on (e) refers to (e–k). High quality figures are available online.

Figure 7.

Presumable directions of chromosome rearrangements during karyotype evolution and changes of host plant preferences of Philaenus species. Karyotype alterations occurred several times independently in the genus. High quality figures are available online.