Dynamic karyotype evolution and unique sex determination systems in Leptidea wood white butterflies

Abstract

BackgroundChromosomal rearrangements have the potential to limit the rate and pattern of gene flow within and between species and thus play a direct role in promoting and maintaining speciation. Wood white butterflies of the genus Leptidea are excellent models to study the role of chromosome rearrangements in speciation because they show karyotype variability not only among but also within species. In this work, we investigated genome architecture of three cryptic Leptidea species (L. juvernica, L. sinapis and L. reali) by standard and molecular cytogenetic techniques in order to reveal causes of the karyotype variability.ResultsChromosome numbers ranged from 2n = 85 to 91 in L. juvernica and 2n = 69 to 73 in L. sinapis (both from Czech populations) to 2n = 51 to 55 in L. reali (Spanish population). We observed significant differences in chromosome numbers and localization of cytogenetic markers (rDNA and H3 histone genes) within the offspring of individual females. Using FISH with the (TTAGG)n telomeric probe we also documented the presence of multiple chromosome fusions and/or fissions and other complex rearrangements. Thus, the intraspecific karyotype variability is likely due to irregular chromosome segregation of multivalent meiotic configurations. The analysis of female meiotic chromosomes by GISH and CGH revealed multiple sex chromosomes: W1W2W3Z1Z2Z3Z4 in L. juvernica, W1W2W3Z1Z2Z3 in L. sinapis and W1W2W3W4Z1Z2Z3Z4 in L. reali.ConclusionsOur results suggest a dynamic karyotype evolution and point to the role of chromosomal rearrangements in the speciation of Leptidea butterflies. Moreover, our study revealed a curious sex determination system with 3–4 W and 3–4 Z chromosomes, which is unique in the Lepidoptera and which could also have played a role in the speciation process of the three Leptidea species.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0375-4) contains supplementary material, which is available to authorized users.

Lack of gene flow: Narrow and dispersed differentiation islands in a triplet of Leptidea butterfly species

“…Within L. sinapis , there was limited genetic differentiation between the Swedish (2n = 57, 58) and the Kazakhstan populations (2n = 56–64) despite being separated by a geographic distance > 4,000 km, while both of these populations were considerably differentiated from the Spanish population (2n = 106, 108). This suggests that the chromosome number cline observed across Eurasia for this species (Dincă et al, , ; Šíchová et al, , ) likely has evolved as a consequence of secondary contact after separation in discrete glacial refugia. A hypothetical but straightforward scenario could be that the ancestral population—probably harbouring a karyotype similar to the ancestral Lepidoptera type (2n approximately = 60; Ahola et al, ) as seen in the sister species, L. reali (2n = 52–54)—was widespread across Eurasia and that glacial intervals forced individuals to refugia in both the Iberian Peninsula and south‐central Asia.…”

“…Overall, the species in the complex are distributed over a vast geographic range (Figure ), covering a wide variety of habitats. They exhibit complex differences in life history characteristics, pupal and genital morphology, mating behaviour, pheromone profiles, habitat preference, karyotype set‐up and genome size (Dincă et al, , ; Freese & Fiedler, ; Friberg, ; Friberg, Olofsson, Berger, Karlsson, & Wiklund, ; Friberg, Vongvanich, et al, ; Friberg & Wiklund, ; Lorkovic, ; Lukhtanov, Dincă, Talavera, & Vila, ; Šíchová et al, ; Talla, Suh, et al, ; Wiklund, , ). Moreover, both L. sinapis and L. juvernica are further subdivided into multiple geographically distinct ecotypes with complex habitat utilization preferences and life history characteristics, potentially reflecting variation in environmental conditions across the distribution ranges (Friberg, Leimar, & Wiklund, ; Friberg, Olofsson, et al, ; Friberg & Wiklund, , ).…”

“…Moreover, both L. sinapis and L. juvernica are further subdivided into multiple geographically distinct ecotypes with complex habitat utilization preferences and life history characteristics, potentially reflecting variation in environmental conditions across the distribution ranges (Friberg, Leimar, & Wiklund, ; Friberg, Olofsson, et al, ; Friberg & Wiklund, , ). Leptidea sinapis also shows striking intraspecific chromosome number variation present in a cline with a gradual increase from 2 n ≈ 56–58 in the northern and eastern parts (Scandinavia–Kazakhstan) to 2 n ≈ 106–108 in the southwestern parts (Iberia) of the distribution range (Dincă et al, , ; Šíchová et al, , ). The exact mechanism behind this karyotype variation is unknown, but both visual inspection of metaphase spreads (Lukhtanov et al, ) and genome size analysis (Talla, Suh, et al, ) strongly suggest that this is a result of a large number of chromosome fissions/fusions rather than whole or partial genome duplications.…”

A new butterfly species from south Russia revealed through chromosomal and molecular analysis of the Polyommatus (Agrodiaetus) damonides complex (Lepidoptera, Lycaenidae)

“…Previously, the low or no underdominance of chromosomal fusions/fissions was demonstrated for butterflies of the genus Leptidea Billberg, 1820 (Lukhtanov et al 2011, Šíchová et al 2015, 2016). In the Agrodiaetus subgenus the low underdominance of chromosomal fusions/fissions was indirectly demonstrated through analysis of homoploid hybrid speciation in P. karindus-P. morgani-P. peilei species complex (Lukhtanov et al 2015b).…”

“…1) COI differentiation. Fusions and fissions of chromosomes are the most probable rearrangements driving the chromosome number change in the P. damonides complex as well as in other butterfly species (Lukhtanov et al 2011, Šíchová et al 2015, 2016). In P. ninae , P. damonides gilanensis , P. arasbarani and P. lukhtanovi some of these fusions/fissions are found in heterozygous conditions resulting in trivalent formation at the MI stage.…”