Abstract Abstract
Lepidoptera (butterflies and moths), as many other groups of animals and plants, simultaneously represent preservation of ancestral karyotype in the majority of families with a high degree of chromosome number instability in numerous independently evolved phylogenetic lineages. However, the pattern and trends of karyotype evolution in some Lepidoptera families are poorly studied. Here I provide a survey of chromosome numbers in skippers (family Hesperiidae) based on intensive search and analysis of published data. I demonstrate that the majority of skippers preserve the haploid chromosome number n=31 that seems to be an ancestral number for the Hesperiidae and the order Lepidoptera at whole. However, in the tribe Baorini the derived number n=16 is the most typical state which can be used as a (syn)apomorphic character in further phylogenetic investigations. Several groups of skippers display extreme chromosome number variations on within-species (e.g. the representatives of the genus Carcharodus Hübner, [1819]) and between-species (e.g. the genus Agathymus Freeman, 1959) levels. Thus, these groups can be used as model systems for future analysis of the phenomenon of chromosome instability. Interspecific chromosomal differences are also shown to be useful for discovering and describing new cryptic species of Hesperiidae representing in such a way a powerful tool in biodiversity research. Generally, the skipper butterflies promise to be an exciting group that will significantly contribute to the growing knowledge of patterns and processes of chromosome evolution.
Keywords: Lepidoptera, Hesperiidae, karyotype evolution, chromosome number, cryptic species, phylogeny, chromosomal conservatism, chromosomal instability
Introduction
The main karyotypic features of organisms, particularly the number of chromosomes, tend to be stable within species (White 1973, King 1993). New chromosomal rearrangements usually originate as heterozygotes and are often – although not always (Lukhtanov et al. 2011) – associated with heterozygote disadvantage. The spread of such rearrangements to fixation within a large population has low probability (King 1993). Therefore, many organisms are characterized by chromosomal conservatism, a situation in which all closely related taxa demonstrate the same chromosome number.
In contrast to chromosomal conservatism, chromosomal instability characterizes situations where multiple closely related taxa (populations, subspecies and/or species) belonging to a single phylogenetic lineage differ drastically from each other by major chromosomal rearrangements, sometimes resulting in high variability in chromosome number.
Both phenomena - chromosomal conservatism and chromosomal instability - are clearly expressed in insects of the order Lepidoptera (butterflies and moths). The modal haploid number of chromosomes (n) of n = 31 or n = 30 (Suomalainen 1969, Lukhtanov 2000) is preserved in the majority of lepidopteran families (Robinson 1971). At the same time, numerous cases of chromosomal instability have been discovered in the butterfly families, e.g. in Papilionidae (Emmel et al. 1995), Pieridae (Lukhtanov 1991, Lukhtanov et al. 2011, Dinca et al. 2011), Nymphalidae (Brown et al. 1992, 2004, 2007a, 2007b) and Riodinidae (Brown et al. 2012). This phenomenon was analyzed in more detail in the family Lycaenidae (Kandul et al. 2004, 2007, Lukhtanov et al. 2005, 2006, 2008, Vershinina and Lukhtanov 2010, 2013, Vila et al. 2010, Talavera et al. 2013, Przybyłowicz et al. 2014).
Skippers (the family Hesperiidae) are studied to a lesser extent with the respect of karyotype evolution than the other butterfly families mentioned above (but see: Emmel and Trew 1973, Saura et al. 2013). This family includes about 4000 species under 567 genera and is a globally distributed group found in all continents except Antarctica (Warren et al. 2008). The tribal level classification of skippers, based on combined analysis of molecular and morphological data, was recently elaborated by Warren and colleagues (Warren et al. 2008, 2009).
Here I provide a first world-wide survey of chromosome numbers in skippers based on intensive search and analysis of published data.
Results
The results of literature search are presented in the Table below. It includes all the discovered chromosome counts except n=13 for Ochlodes venatus (Bremer et Grey, 1853), noted by Bigger (1960) as “Augiades venata”. The name Ochlodes venatus was long used for the Ochlodes species of Europe, but it actually refers to its Far Eastern sister species, and the European taxon is now called Ochlodes sylvanus (Esper, 1777) (ICZN 2000). Both European and Far Eastern species have the same chromosome number n=29 (Federley 1938, Lorković 1941, Abe et al. 2006), not n=13 as indicated by Bigger (1960). Thus, the species name used by Bigger (1960) was probably misidentification.
The classification of skippers accepted in this paper follows Warren and colleagues (Warren et al. 2008, 2009).
Discussion
Modal chromosomal numbers
The table gives the chromosome numbers of 205 species of skippers, i.e. about 5% of the species of the world fauna. This number is not enough to infer any final statements about peculiarities of chromosome numbers distribution within the Hesperiidae. However, several tentative conclusions can be made. The haploid chromosome number n=31 was found in 50 studied species of skippers and, thus, it is a clear modal number for the family at whole. Interestingly, n=31 was found in representatives of all investigated subfamilies, except for Heteropterinae. However, in the last subfamily only one species was karyologically studied until now, and discovery of n=31 in Heteropterinae is not excluded in future. The next most common numbers are n=29 (43 species), n=30 (33 species) and n=28 (13 species).
Subfamilies Coeliadinae and Eudaminae have a sharp peak at n=31. In the subfamily Trapezitinae n=31 was also found (only one species studied).
Within the subfamily Pyrginae, the modal number n=31 is found in the tribe Erynnini. The tribe Pyrrhopygini is characterized by the most common n=28. The modal number in the tribe Tagiadini is n=30. The tribe Carcharodini has peaks at n=30 and n=31. In the tribe Pyrgini, n=29, n=30 and n=31 were found as the most common numbers.
In the family Heteropterinae n=29 was found (only one species studied).
Within the subfamily Hesperiinae, the tribes Taractrocerini, Thymelicini, Calpodini, Moncini and Hesperiini are characterized by the most common n=29. Very variable chromosome numbers (from n=5 to n=50) were found in the tribe Aeromachini. It is difficult to infer the modal number for the last tribe. However, it should be noted that one species, Thoressa varia, has n=31 as the majority of other skippers. The tribe Baorini (subfamily Hesperiinae) has a clear peak at n=16, so it is exceptional with respect to the modal number of chromosomes.
The overall evidence indicates that chromosome numbers of Coeliadinae, Eudaminae, Trapezitinae, Pyrginae and Hesperiinae conform to the lepidopteran modal of n=31 (Robinson 1971). This number seems to be an ancestral one for the Hesperiidae as for the order Lepidoptera at whole (Suomalainen 1969, Lukhtanov 2000). This modal number (or its deviation to n=30, n=29 and 28) were preserved in the majority of skippers. However, in the tribe Baorini the number n=16 was evolved and, thus, represents a derived trait which can be used as a (syn)apomorphic character in further phylogenetic studies of the family Hesperiidae.
Between- and within-species variations in chromosome number
Several groups of skippers display extreme chromosome number variations at the within-species level (Table). The most extreme variations in number of chromosome elements were observed in first meiotic metaphase of Carcharodus boeticus, Carcharodus dravira and Carcharodus flocciferus (Table, de Lesse 1960). The nature of these variations remains unknown, and there are two plausible explanations for this phenomenon. First, this variation can be explained by presence of so-called B-chromosomes (=additional chromosomes, =supernumerary chromosomes) (de Lesse 1960). B-chromosomes consist mainly of repetitive DNA and can sometimes accumulate through processes of mitotic or meiotic drive (Jones et al. 2008). B-chromosomes can be distinguished from normal A-chromosomes because they are usually smaller and can be seen as additional chromosomes present in only some of the individuals in a population (Camacho et al. 2000, Jones et al. 2008).
Second, this kind of variation can be caused by violations in meiotic chromosome pairing resulting in appearance of univalents (instead of bivalents) in meiotic prophase (Lorković 1990). This type of variation was studied in detail by Maeki and Ae (1979) in butterfly genus Papilio and is expected if regular or irregular interspecific mating occurs in nature. Anyway, the nature of intraspecific variations observed in Carcharodus is different from that discovered in the Wood White butterfly Leptidea sinapis (Linnaeus, 1758) (Pieridae). In the last species the compared range of intraspecific variation in chromosome number (from n=28 to n=53) was caused by multiple chromosome fusions/fissions accumulated within the species (Lukhtanov et al. 2011, Dinca et al. 2011).
Between-species variation exists in numerous genera of skippers (Table 1) and is especially expressed in the Nearctic genus Agathymus Freeman, 1959, in which the range of haploid numbers was discovered from n =5 in Agathymus aryxna to n=38 in Agathymus alliae (Freeman 1969). This range is comparable of even exceeds the range found in chromosomally diverse genera from other butterfly families (Lorković 1990, Lukhtanov et al. 2005, Talavera et al. 2013). Thus, the genera of Hesperiidae can be used as model systems for future analysis of the phenomenon of chromosome instability.
Table 1.
# | Species | Haploid chromosome number | Country | Reference |
---|---|---|---|---|
Subfamily Coeliadinae | ||||
1 | Bibasis aquilina (Speyer, 1879) | 29 | Japan | Maeki 1953 |
Bibasis aquilina chrysaeglia (Butler, 1881) | 31 (2n=62) | Japan | Abe et al. 2006 | |
2 | Bibasis jaina formosana Fruhstorfer, 1911 | 31 | Taiwan | Maeki and Ae 1968b |
3 | Choaspes benjaminii (Guérin-Méneville, 1843) | 31 | Japan | Maeki 1953 |
Choaspes benjaminii japonica (Murray, 1875) | 31 | Japan | Saitoh et al. 1978 | |
4 | Coeliades anchises jucunda (Butler, 1881) | 30 | Oman | Saitoh 1982 |
5 | Coeliades ernesti (Grandidier, 1867) | 31 | Madagascar | de Lesse 1972 |
6 | Coeliades fervida (Butler, 1880) | 23 | Madagascar | de Lesse 1972 |
7 | Coeliades forestan arbogastes (Guenee, 1863) | 31 | Madagascar | de Lesse 1972 |
8 | Coeliades ramanatek (Boisduval, 1833) | 31 | Madagascar | de Lesse 1972 |
Subfamily Euschemoninae no chromosomal data available | ||||
Subfamily Eudaminae | ||||
9 | Achalarus casica (Herrich-Schäffer, 1869) | 29 | USA (Texas) | Emmel and Trew 1973 |
10 | Achalarus lyciades (Geyer, 1832) | 31 | USA (Connecticut) | Maeki 1961 |
11 | Achalarus toxeus (Plötz, 1882) | 16 | Mexico | Maeki and Remington 1960 |
12 | Astraptes anaphus (Godman et Salvin, 1896) | 31 | Bolivia | de Lesse 1967a |
13 | Astraptes fulgerator (Walch, 1775) | 31 | Peru | Kumagai et al. 2010 |
14 | Astraptes naxos (Hewitson, 1867) | 31 | Brazil | Saura et al. 2013 |
15 | Astraptes phalaecus (Godman et Salvin, 1893) | 25 | Guatemala | de Lesse 1967a |
16 | Astraptes longipennis (Plötz, 1882) | 31 | Costa Rica | Kumagai et al. 2010 |
31 | Peru | Kumagai et al. 2010 | ||
31 | Brazil | Kumagai et al. 2010 | ||
17 | Autochton sp. | 20, 21 | Brazil | Kumagai et al. 2010 |
18 | Chioides albofasciatus (Hewitson, 1867) | 31 | Mexico | de Lesse 1970a |
Chioides albofasciatus (Hewitson, 1867) (as Chioides catillus) | 31 | Mexico | Maeki and Remington 1960 | |
Chioides albofasciatus (Hewitson, 1867) | 31 | USA (Texas) | Emmel and Trew 1973 | |
19 | Entheus priassus pralina Evans, 1952 | 22 | Brazil | Saura et al. 2013 |
20 | Epargyreus barisses (Hewitson, 1874) | 31 | Argentina | de Lesse 1967 |
21 | Epargyreus clarus (Cramer, 1775) | 31 | USA (Florida) | Maeki 1961 |
22 | Epargyreus clavicornis tenda Evans, 1955 | ca 29–30 | Guatemala | de Lesse 1970a |
23 | Oechydrus chersis (Herrich-Schäffer, 1869) | 31 | Bolivia | de Lesse 1967a |
24 | Phocides polybius phanias (Burmeister, 1880) | 16 | Brazil | Saura et al. 2013 |
25 | Tarsoctenus praecia plutia (Hewitson, 1857) | 15 | Brazil | Saura et al. 2013 |
26 | Thorybes pylades pylades (Scudder, 1870) | 31 | USA (Connecticut) | Maeki 1961 |
27 | Udranomia spitzi (Hayward, 1942) | 29 | Brazil | de Lesse and Brown 1971 |
28 | Urbanus dorantes dorantes (Stoll, 1790) | 31 | Mexico | de Lesse 1970a |
29 | Urbanus doryssus doryssus (Swainson, 1831) | 14 | Costa Rica | Kumagai et al. 2010 |
30 | Urbanus proteus (Linnaeus, 1758) | 31 | Bolivia | de Lesse 1967a |
31 | Mexico | de Lesse 1970a | ||
31 | USA (Florida) | Maeki 1961 | ||
31 | Urbanus simplicius (Stoll, 1790) | 31 | Argentina | de Lesse 1967a |
32 | Urbanus teleus (Hübner, 1821) | 31 | Argentina | de Lesse 1967a |
Subfamily Pyrginae | ||||
Tribe Pyrrhopygini | ||||
33 | Elbella lamprus (Hopffer, 1874) | 40 | Brazil | de Lesse 1970a |
34 | (?) Jemadia sp. | 32(?) | Brazil | Saura et al. 2013 |
35 | Mimoniades montana J. Zikán, 1938 | 27 | Brazil | Saura et al. 2013 |
36 | Mimoniades nurscia (Swainson, 1821) | 28 | Ecuador | de Lesse 1967a |
Mimoniades nurscia malis (Godman et Salvin, 1879) | 28 | Colombia | Saura et al. 2013 | |
37 | Mimoniades sp. | 21 | Colombia | Saura et al. 2013 |
38 | Mimoniades sp. | 28 | Colombia | Saura et al. 2013 |
39 | Mimoniades versicolor (Latreille, [1824]) | 28 | Brazil | de Lesse and Brown 1971 |
40 | Pyrrhopyge charybdis Westwood, 1852 | 14(?) | Brazil | Saura et al. 2013 |
41 | Pyrrhopyge pelota Plötz, 1879 | 28 | Argentina | de Lesse 1967a |
42 | Pyrrhopyge sp. | 15 | Brazil | Saura et al. 2013 |
43 | Sarbia sp. | 30 | Brazil | Saura et al. 2013 |
Tribe Tagiadini | ||||
44 | Daimio tethys (Ménétriés, 1857) | 30 | Japan | Maeki 1953, Maeki and Makino 1953 |
45 | Daimio tethys moorei Mabille, 1876 | 30 | Taiwan | Maeki and Ae 1968b |
46 | Eagris lucetia (Hewitson, 1876) | 30 | Uganda | de Lesse 1968 |
47 | Eagris sabadius astoria Holland, 1896 | 30 | Kenya | de Lesse 1968 |
48 | Eretis lugens (Rogenhofer, 1891 | 28 | Kenya | de Lesse 1968 |
Tribe Celaenorrhinini | ||||
49 | Sarangesa phidyle (Walker, 1870) | 29 | Senegal | de Lesse and Condamin 1962 |
Tribe Carcharodini | ||||
50 | Carcharodus alceae (Esper, [1780]) | 31 | Croatia | Lorković 1941 |
51 | Carcharodus boeticus Reverdin, 1913 | 43–47 | Spain | de Lesse 1960 |
Carcharodus boeticus Reverdin, 1913 | 40–52 | France | de Lesse 1960 | |
Carcharodus boeticus Reverdin, 1913 | 38–46 | Italy | de Lesse 1960 | |
52 | Carcharodus dravira (Moore, 1874) | 37–48 (with Us) | Iran | de Lesse 1960 |
53 | Carcharodus flocciferus (Zeller, 1847) | 32–41 (with Us) | France (Cauterets) | de Lesse 1960 |
54 | Carcharodus flocciferus (Zeller, 1847) | 42–58 (with Us) | Italy | de Lesse 1960 |
55 | Carcharodus lavatherae (Esper, [1783]) | 30 | France (Salau, Ariege) | de Lesse 1960 |
56 | Carcharodus orientalis Reverdin, 1913 | 31–32 | Lebanon | de Lesse 1960 |
30 | Turkey (Van) | de Lesse 1960 | ||
30–37 (with Us) | Turkey (Amasya) | de Lesse 1960 | ||
57 | Carcharodus stauderi ambiguus Verity, 1925 | 30 | Lebanon | de Lesse 1960 |
30 | Turkey | de Lesse 1960 | ||
58 | Hesperopsis alpheus (W. H. Edwards, 1876) (as Pholisora) | 34 | USA (Texas) | Emmel and Trew 1973 |
59 | Muschampia nomas (Lederer, 1855) | 30 | Lebanon | de Lesse 1960 |
60 | Muschampia proteides (Wagner, 1929) | 30 | Lebanon | Larsen 1975 |
61 | Muschampia proto (Ochsenheimer, 1808) | 30 | Spain | de Lesse 1960 |
30 | Lebanon | Larsen 1975 | ||
62 | Pholisora catullus (Fabricius, 1793) | 29 | ?USA | Lorković in Robinson 1971 |
63 | Spialia orbifer (Hübner, [1823]) | 30 | Croatia | Lorković 1941 |
31 | Turkey | de Lesse 1960 | ||
64 | Spialia phlomidis (Herrich-Schäffer, [1845]) | 31 | Turkey | de Lesse 1960 |
65 | Spialia sertorius (Hoffmannsegg, 1804) | 31 | Slovenia | Lorković 1941 |
Tribe Erynnini | ||||
66 | Chiomara asychis georgina (Reakirt, 1868) | 31 | Mexico | de Lesse 1970a |
Chiomara asychis georgina (Reakirt, 1868) | 32 | USA (Texas) | Emmel and Trew 1973 | |
67 | Chiomara sp. | 31 | Trinidad | Wesley and Emmel 1975 |
68 | Ebrietas anacreon (Staudinger, 1876) | 31 | Argentina | de Lesse 1967a |
69 | Ebrietas osyris (Staudinger, 1876) | 31 | Argentina | de Lesse 1967a |
70 | Erynnis baptisiae (W. Forbes, 1936) | 31 | USA (Connecticut) | Maeki 1961 |
71 | Erynnis funeralis (Scudder et Burgess, 1870) | 31 | Argentina | de Lesse 1967a |
72 | Erynnis horatius (Scudder et Burgess, 1870) | 31 | USA (Florida) | Maeki 1961 |
73 | Erynnis icelus (Scudder et Burgess, 1870) | 30 | USA (Connecticut) | Maeki 1961 |
74 | Erynnis juvenalis juvenalis (Fabricius, 1793) | 30 | USA (Connecticut) | Maeki 1961 |
75 | Erynnis lucilius (Scudder et Burgess, 1870) | 31 | USA (Connecticut) | Maeki and Remington 1960a |
76 | Erynnis marloyi (Boisduval, [1834]) | 31 | Lebanon | de Lesse 1960 |
77 | Erynnis montanus (Bremer, 1861) | 31 (2n=62) | Japan | Abe et al. 2006 |
Erynnis montanus (Bremer, 1861) | 31 | Japan | Maeki 1953 | |
78 | E. persius (Scudder, 1863) | 31 | USA (Connecticut) | Maeki 1961 |
79 | Erynnis tages (Linnaeus, 1758) | 31 | Croatia | Lorković 1941 |
31 | France | de Lesse 1960 | ||
31 | England | Bigger 1960 | ||
80 | Erynnis tristis tatius (W. H. Edwards, 1883) | 31 | USA (Texas) | Emmel and Trew 1973 |
81 | Gesta gesta (Herrich-Schäffer, 1863) | 32 | Tobago | Wesley and Emmel 1975 |
82 | Grais stigmaticus (Mabille, 1883) | 31 | Mexico | Maeki and Remington 1960a |
83 | Theagenes albiplaga (C. Felder et R. Felder, 1867) | 31 | Bolivia | de Lesse 1967a |
Tribe Achlyodidini | ||||
84 | Achlyodes pallida (R. Felder, 1869) (as Achlyodes selva) | 15 | Bolivia | de Lesse 1967a |
15 | Mexico | de Lesse 1970a | ||
85 | Zera zera zera (Butler, 1870) | 34 | Brazil | de Lesse and Brown 1971 |
Tribe Pyrgini | ||||
86 | Anisochoria sublimbata Mabille, 1883 | 31 | Argentina | de Lesse 1967a |
87 | Antigonus erosus (Hübner, [1812]) | 31 | Mexico | de Lesse 1970a |
88 | Antigonus liborius Plötz, 1884 | 31 | Argentina | de Lesse 1967a |
89 | Celotes nessus (W. H. Edwards, 1877) | 14, 13 | USA (Texas) | Emmel and Trew 1973 |
90 | Heliopetes arsalte (Linnaeus, 1758) | 30 | Bolivia | de Lesse 1967a |
Heliopetes arsalte (Linnaeus, 1758) | 30 | Mexico | de Lesse 1970a | |
91 | Heliopetes laviana (Hewitson, 1868) | 29 | USA (Texas) | Emmel and Trew 1973 |
92 | Heliopetes macaira (Reakirt, [1867]) | 29 | USA (Texas) | Emmel and Trew 1973 |
93 | Heliopetes omrina (Butler, 1870) | 30 | Argentina | de Lesse 1967a |
94 | Heliopyrgus americanus (Blanchard, 1852) | 30 | Chile | de Lesse 1967a |
95 | Paches loxus (Westwood, [1852]) | 31 | Guatemala | de Lesse 1970a |
96 | Pyrgus aladaghensis De Prins et van der Poorten, 1995 | ca 18–21 | Turkey | Lukhtanov and Kandul 1995 (in Hesselbarth et al. 1995) |
97 | Pyrgus albescens Plötz, 1884 | 30 (2n=60) | USA (Texas) | Goodpasture 1976 |
Pyrgus albescens Plötz, 1884 | 28 | USA (Texas) | Emmel and Trew 1973 | |
98 | Pyrgus alveus (Hübner, [1803]) | 24 | Finland | Federley 1938 |
24 | Croatia | Lorković 1941 | ||
24 | Turkey | Lukhtanov and Kandul 1995 (in Hesselbarth et al. 1995) | ||
99 | Pyrgus bellieri (Oberthür, 1910) | 27 | France | de Lesse 1960 |
100 | Pyrgus bocchoris (Hewitson, 1874) | 30 | Argentina | de Lesse 1967a |
101 | Pyrgus bolkariensis De Prins et van der Poorten, 1995 | 30 | Turkey | Lukhtanov and Kandul 1995 (in Hesselbarth et al. 1995) |
102 | Pyrgus cacaliae (Rambur, 1839) | 30 | Italy | de Lesse 1960 |
103 | Pyrgus carlinae (Rambur, [1839]) | 30 | Italy | de Lesse 1960 |
104 | Pyrgus carthami (Hübner, [1813]) | 29 | Italy | de Lesse 1960 |
105 | Pyrgus cirsii (Rambur, [1839]) | 30 | France (Peyreleau, Aveyron) | de Lesse 1960 |
106 | Pyrgus fides Hayward, 1940 | 30 | Chile | de Lesse 1967a |
107 | Pyrgus maculates (Bremer et Grey, 1852) | 31 (2n=62) | Japan | Abe et al. 2006 |
108 | Pyrgus malvae (Linnaeus, 1758) | 31 | Finland | Federley 1938 |
33 | England | Bigger 1960 | ||
109 | Pyrgus oileus (Linnaeus, 1767) | 30 (2n=60) | USA (Texas) | Goodpasture 1976 |
32 | USA (Texas) | Emmel and Trew 1973 | ||
110 | Pyrgus onopordi (Rambur, [1839]) | 30 | France | Lorković 1941 |
111 | Pyrgus serratulae (Rambur, [1839]) | 30 | France | Lorković 1941 |
112 | Trina geometrina geometrina (C. Felder et R. Felder, 1867) | 31 | Brazil | de Lesse and Brown 1971 |
Subfamily Heteropterinae | ||||
113 | Butleria quilla Evans, 1939 | 29 | Chile | de Lesse 1967a |
Subfamily Trapezitinae | ||||
114 | Trapezites eliena Hewitson, 1868 | 31 | Australia | Maeki and Ogata 1971 |
Subfamily Hesperiinae | ||||
Tribe Aeromachini | ||||
115 | Aegiale hesperiaris (Walker, 1856) | 24 | Mexico | Freeman 1969 |
116 | Agathymus alliae (Stallings et Turner, 1957) | 38 | USA (Arizona) | Freeman 1969 |
117 | Agathymus aryxna (Dyar, 1905) | 5 | Mexico | Freeman 1969 |
118 | Agathymus baueri (Stallings et Turner, 1954) | 15 | USA (Arizona) | Freeman 1969 |
119 | Agathymus chisosensis (Freeman, 1952) | 18 | USA (Texas) | Freeman 1969 |
120 | Agathymus estelleae valverdiensis Freeman, 1966 | 9 | USA (Texas) | Freeman 1969 |
Agathymus estelleae estelleae (Stallings et Turner, 1958) | 9 | Mexico | Freeman 1969 | |
121 | Agathymus freemani Stallings, Turner et Stallings, 1960 | 15 | USA (Arizona) | Freeman 1969 |
122 | Agathymus gilberti Freeman, 1964 | 21 | USA (Texas) | Freeman 1969 |
123 | Agathymus mariae chinatiensis Freeman, 1964 | 22 | USA (Texas) | Freeman 1969 |
Agathymus mariae lajitaensis Freeman, 1964 | 22 | USA (Texas) | Freeman 1969 | |
Agathymus mariae mariae (Barnes et Benjamin, 1924) | 22 | USA or Mexico | Freeman 1969 | |
Agathymus mariae rindgei Freeman, 1964 | 22 | USA (Texas) | Freeman 1969 | |
124 | Agathymus micheneri Stallings, Turner et Stallings, 1961 | 20 | Mexico | Freeman 1969 |
125 | Agathymus neumoegeni florenceae (Stallings et Turner, 1957) | 10 | USA (Texas) | Freeman 1969 |
Agathymus neumoegeni macalpinei (Freeman, 1955) | 10 | USA (Texas) | Freeman 1969 | |
126 | Agathymus polingi (Skinner, 1905) | 10 | USA (Arizona) | Freeman 1969 |
127 | Agathymus remingtoni (Stallings et Turner, 1958) | 9 | Mexico | Freeman 1969 |
128 | Alera vulpina (C. Felder et R. Felder, 1867) | ca27 | Ecuador | de Lesse 1967a |
129 | Ankola fan (Holland, 1844) | 10 | Uganda | De Lesse 1968 |
130 | Arotis derasa (Herrich-Schäffer, 1870) (as Euphyes) | 28 | Brazil | de Lesse and Brown 1971 |
131 | Erionota thrax thrax (Linnaeus, 1767) | 29 | Malaysia | Saitoh and Kumagai 1974 |
132 | Euphyes leptosema Mabille, 1891 | ca28 | Argentina | de Lesse 1967a |
133 | Megathymus coloradensis coloradensis Riley, 1877 | 27 | USA | Freeman 1969 |
134 | Megathymus coloradensis kendalli Freeman, 1965 | 27 | USA (South central Texas) | Freeman 1969 |
Megathymus coloradensis louiseae Freeman, 1963 | 27 | USA (Western Texas) | Freeman 1969 | |
Megathymus coloradensis navajo Skinner, 1911 | 27 | USA | Freeman 1969 | |
Megathymus coloradensis reinthali Freeman, 1963 | 27 | USA (Texas) | Freeman 1969 | |
Megathymus coloradensis reubeni Stallings, Turner et Stallings, 1963 | 27 | USA (Texas) | Freeman 1969 | |
Megathymus coloradensis stallingsi Freeman, 1943 | 27 | USA | Freeman 1969 | |
Megathymus coloradensis wilsonorum Stallings et Turner, 1958 | 27 | ?Mexico | Freeman 1969 | |
135 | Megathymus violae Stallings et Turner, 1956 | 27 | USA | Maeki 1961, Freeman 1969 |
136 | Megathymus yuccae buchholzi Freeman, 1952 | 26 | USA (Florida) | Freeman 1969 |
137 | Pardaleodes incerta (Snellen, 1872) | 17 | Uganda | de Lesse 1968 |
138 | Stallingsia maculosus (Freeman, 1955) | 50 | USA (Texas) | Maeki 1961, Freeman 1969 |
139 | Suastus gremius (Fabricius, 1798) | 23 | Taiwan | Maeki and Ae 1968b |
140 | Thoressa varia (Murray, 1875) | 31 (2n=62) | Japan | Abe et al. 2006 |
141 | Thoressa varia (Murray, 1875) | 31 | Japan | Maeki 1953 |
Tribe Baorini | ||||
142 | Gegenes gambica (Mabille, 1878) | 41 | Yemen | Saitoh 1984 |
41 | Turkey | de Lesse 1960 | ||
41 | Lebanon | Larsen 1982 | ||
143 | Gegenes nostrodamus (Fabricius, 1793) | 15 | Egypt | Larsen 1982 |
15 | Israel | Saitoh 1979, Larsen 1982 | ||
144 | Gegenes pumilio (Hoffmansegg, 1804) | 24 | France | de Lesse 1960 |
24 | Alger | de Lesse 1967b | ||
145 | Parnara guttata (Bremer et Grey, 1852) | 16 | Japan | Maeki 1953, Maeki and Makino 1953 |
16 | China | Saitoh and Abe 1981 | ||
146 | Pelopidas conjucta conjucta (Herrich-Schäffer, 1869) | 16 | Hong Kong | Maeki and Ae 1968a |
147 | Pelopidas jansonis (Butler, 1878) | 16 (2n=32) | Japan | Abe et al. 2006 |
148 | Pelopidas mathias (Fabricius, 1798) | 16 | Japan | Maeki and Remington 1960 |
149 | Pelopidas thrax (Hübner, [1821]) | 16 | Lebanon | Larsen 1975 |
150 | Polytremis lubricans (Herrich-Schäffer, 1869) | 16 | Taiwan | Maeki and Ae 1968b |
151 | Polytremis pellucida (Murray, 1875) | 16, 17, 18 (2n=32, 33) | Japan | Abe et al. 2006 |
16 | Japan | Maeki and Remington 1960 | ||
152 | Zenonia zeno (Trimen, 1864) | 16 | Uganda | de Lesse 1968 |
Tribe Taractrocerini | ||||
153 | Ocybadistes walkeri sothis Waterhouse, 1933 | 28 | Australia | Maeki and Ogata 1971 |
154 | Potanthus flavus (Murray, 1875) | 29 (2n=58) | Japan | Abe et al. 2006 |
155 | Telicota ancilla horisha Evans, 1934 | 29 | Taiwan | Maeki and Ae 1968b |
156 | Telicota colon stinga Evans, 1949 | 29 | Japan (Okinava) | Abe et al. 2006 |
157 | Telicota ohara formosana Fruhstorfer, 1911 | 29 (2n=58) | Taiwan | Abe et al. 2006 |
Tribe Thymelicini | ||||
158 | Copaeodes minima (W.H. Edwards, 1870) | 29 | USA (Florida) | Maeki 1961 |
159 | Thymelicus sylvestris (Poda, 1761) | 27 | England | Bigger 1960 |
160 | Thymelicus sylvaticus (Bremer, 1861) | 10 (2n=20) | Japan | Abe et al. 2006 |
161 | Thymelicus acteon (Rottemburg, 1775) | 28 | Spain | de Lesse 1970c |
162 | Thymelicus hyrax (Lederer, 1861) | 29 | Lebanon | Larsen 1975 |
163 | Thymelicus leoninus (Butler, 1878) | 9 (2n=18) | Japan | Abe et al. 2006 |
164 | Thymelicus lineola (Ochsenheimer, 1808) | 29 | Finland | Federley 1938 |
29 | Lebanon | Larsen 1975 | ||
Tribe Calpodini | ||||
165 | Ebusus ebusus (Cramer, [1780]) | 29 | Mexico | de Lesse 1970a |
166 | Lychnuchus celsus (Fabricius, 1793) | 30 | Brazil | de Lesse and Brown 1971 |
167 | Panoquina hecebolus (Scudder, 1872) | 29 | USA (Texas) | Emmel and Trew 1973 |
168 | Panoquina ocola (W. H. Edwards, 1863) | 29 | USA (Texas) | Emmel and Trew 1973 |
169 | Panoquina panoquin (Scudder, 1863) | 29 | USA (Florida) | Maeki 1961 |
170 | Panoquina panoquinoides (Skinner, 1891) | 29 | USA (Texas) | Emmel and Trew 1973 |
Tribe Anthoptini no chromosomal data available | ||||
Tribe Moncini | ||||
171 | Amblyscirtes aenus W.H. Edwards, 1878 | 28, 29 | USA (Texas) | Emmel and Trew 1973 |
172 | Amblyscirtes cassus W. H. Edwards, 1883 | 29 | USA (Texas) | Emmel and Trew 1973 |
173 | Amblyscirtes celia (Skinner, 1895) | 29 | USA (Texas) | Emmel and Trew 1973 |
174 | Amblyscirtes phylace W.H. Edwards, 1878 | 29 | USA (Texas) | Emmel and Trew 1973 |
175 | Amblyscirtes texanae Bell, 1927 | 29 | USA (Texas) | Emmel and Trew 1973 |
176 | Amblyscirtes vialis (W. H. Edwards, 1862) | 29 | USA (Connecticut) | Maeki 1961 |
177 | Cymaenes sp. | 31 | Tobago | Wesley and Emmel 1975 |
178 | Enosis immaculata immaculata (Hewitson, 1868) | 29 | Ecuador | Kumagai et al. 2010 |
179 | Lerema accius (Smith, 1797) | 29 (2n=58) | USA (Texas) | Goodpasture 1976 |
29 | USA (Texas) | Emmel and Trew 1973 | ||
180 | Moeris vopiscus (Herrich-Schäffer, 1869) | 27 | Peru | Kumagai et al. 2010 |
181 | Nastra lherminier (Latreille, [1824]) | 30 | USA (Connecticut) | Maeki 1961 |
182 |
Thargella
caura (Plötz, 1882) |
25 | Brazil | de Lesse and Brown 1971 |
183 | Vettius coryna (Hewitson, [1866]) | 31, ca32 | Ecuador | de Lesse 1967a |
184 | Vettius phyllus prona Evans, 1955 | 26 | Brazil | de Lesse and Brown 1971 |
185 | Vettius triangularis (Hübner, [1831]) | 26 | Brazil | Kumagai et al. 2010 |
Tribe Hesperiini | ||||
186 | Asbolis capucinus (Lucas, 1857) | 48 | USA (Florida) | Maeki 1961 |
187 | Cynea iquita (Bell, 1941) | 29 | Argentina | de Lesse 1967a |
188 | Hesperia comma (Linnaeus, 1758) | 28 | Italy | de Lesse 1970c |
28 | Lebanon | Larsen 1975 | ||
189 | Hesperia florinda Butler, 1878 | 28 (2n=56) | Japan | Abe et al. 2006 |
190 | Hylephila fasciolata (Blanchard, 1852) | 29 | Argentina | de Lesse 1967a |
191 | Hesperia phyleus (Drury, 1773) | 29 | Argentia | de Lesse 1967a |
29 | USA (Florida) | Maeki 1961 | ||
192 | Hesperia signata (Blanchard, 1852) | 29 | Chile | de Lesse 1967a |
193 | Ochlodes ochraceus (Bremer, 1861) | 29 (2n=58) | Japan | Abe et al. 2006 |
24 | Japan | Maeki and Remington 1960 | ||
194 | Ochlodes sylvanoides (Boisduval, 1852) | 29 | USA | Maeki 1961 |
195 | Ochlodes sylvanus (Esper, 1777) | 29 | Finland | Federley 1938 |
29 | Croatia | Lorković 1941 | ||
196 | Ochlodes venatus (Bremer et Grey, 1853) (as sylvanus Esper, 1777) | 29 (2n=58) | Japan | Abe et al. 2006 |
197 | Oligoria maculata (W. H. Edwards, 1865) | 29 | USA (Florida) | Maeki 1961 |
198 | Poanes hobomok hobomok (Harris, 1862) | 29 | ?USA | Lorković in Robinson 1971 |
199 | Poanes taxiles (W. H. Edwards, 1881) | 29 | USA | Maeki 1961 |
200 | Poanes zabulon (Boisduval et Le Conte, [1837]) (as Polites zabulon) | 29 | USA (Connecticut) | Maeki 1961 |
201 | Polites themistocles (Latreille, [1824]) | 29 | USA (Florida) | Maeki 1961 |
202 | Poanes vibex catilina (Plötz, 1886) | 29 | Argentina | de Lesse 1967a |
Poanes vibex praeceps (Scudder, 1872) | 27 | USA (Texas) | Emmel and Trew 1973 | |
Poanes vibex vibex (Geyer, 1832) | 29 | USA (Florida) | Maeki 1961 | |
203 | Wallengrenia egeremet (Scudder, 1863) | 28 | USA (Texas) | Emmel and Trew 1973 |
204 | Wallengrenia otho curassavica (Snellen, 1887) | 28–30 | USA (Texas) | Emmel and Trew 1973 |
205 | Wallengrenia premnas (Wallengren, 1860) | 27 | Argentina | de Lesse 1967 |
Detecting cryptic species using analysis of chromosomal differences
Recent years karyological data have been widely used in studies of butterfly taxonomy and in biodiversity research as main or additional chracters for detecting cryptic species (e.g. Dinca et al. 2011) and for synonymizing biological entities that were incorrectly described as distinct species (e.g. Vila et al. 2010). The family Hesperiidae is not excluded in this respect. In the genus Gegenes Hübner, [1819], two cryptic species Gegenes pumilio (n=24) and Gegenes gambica (n=41) were discovered through extensive chromosome analysis of different populations (de Lesse 1960, 1967b, Larsen 1982, Saitoh 1984).
In the genus Pyrgus Hübner, [1819], our unpublished chromosome data (see Table) were used to recognize and then to describe two morphologically similar species, Pyrgus bolkariensis and Pyrgus aladaghensis (De Prins and van der Poorten 1995).
Thus, interspecific chromosomal differences are useful for discovering and describing new cryptic species of Hesperiidae representing in such a way a powerful tool in biodiversity research.
Acknowledgements
I thank A. Warren (University of Florida) for help and consultations in taxonomy and nomenclature of skippers. The study was supported by the Russian Foundation for Basic Research: mainly by grant RFBR 13-04-92716-IND-a and partially by grant RFBR 14-04-01051-a.
Citation
Lukhtanov VA (2014) Chromosome number evolution in skippers (Lepidoptera, Hesperiidae). Comparative Cytogenetics 8(4): 275–291. doi: 10.3897/CompCytogen.v8i4.8789
References
- Abe A, Kushibiki M, Kudoh K. (2006) A study of male germ-line chromosomes in 14 species of the Hesperiidae (Lepidoptera). Transactions of the Lepidopterological Society of Japan 57(3): 217–228. [Google Scholar]
- Bigger TRL. (1960) Chromosome numbers of Lepidoptera. Entomologist’s Gazette 11: 149–152. [Google Scholar]
- Brown KS Jr, Emmel TC, Eliazar PJ, Suomalainen E. (1992) Evolutionary patterns in chromosome numbers in neotropical Lepidoptera. I. Chromosomes of the Heliconiini (Family Nymphalidae: Subfamily Nymphalinae). Hereditas 117(2): 109–125. doi: 10.1111/j.1601-5223.1992.tb00165.x [DOI] [PubMed] [Google Scholar]
- Brown KS Jr, Freitas AVL, von Schoultz B, Saura AO, Saura A. (2007a) Chromosomal evolution of South American frugivorous butterflies in the Satyroid clade (Nymphalidae: Charaxinae, Morphinae and Satyrinae). Biological Journal of the Linnean Society 92: 467–481. doi: 10.1111/j.1095-8312.2007.00872.x [Google Scholar]
- Brown KS Jr, Freitas AVL, Wahlberg N, von Schoultz B, Saura AO, Saura A. (2007b) Chromosomal evolution in the South American Nymphalidae. Hereditas 144(4): 137–148. doi: 10.1111/j.2007.0018-0661.02015.x [DOI] [PubMed] [Google Scholar]
- Brown KS Jr, von Schoultz B, Suomalainen E. (2004) Chromosome evolution in Neotropical Danainae and Ithomiinae (Lepidoptera). Hereditas 141(3): 216–236. doi: 10.1111/j.1601-5223.2004.01868.x [DOI] [PubMed] [Google Scholar]
- Brown KS Jr, von Schoultz B, Saura AO, Saura A. (2012) Chromosomal evolution in the South American Riodinidae (Lepidoptera: Papilionoidea). Hereditas 149(4): 128–138. doi: 10.1111/j.1601-5223.2012.02250.x [DOI] [PubMed] [Google Scholar]
- Camacho JPM, Sharbel TF, Beukeboom LW. (2000) B-chromosome evolution. Philosophical Transactions of the Royal Society London B 355: 163–178. doi: 10.1098/rstb.2000.0556 [DOI] [PMC free article] [PubMed] [Google Scholar]
- de Lesse H. (1960) Spéciation et variation chromosomique chez les Lépidoptères Rhopalocères. Annales des Sciences Naturelles (Ser. 12) 2: 1–223. [Google Scholar]
- de Lesse H. (1967a) Les nombres de chromosomes chez les Lépidoptères Rhopalocères néotropicaux. Annales de la Societe Entomologique de France (NS) 3: 67–136. [Google Scholar]
- de Lesse H. (1967b) Formules chromosomiques de Lépidoptères Rhopalocères d’Afrique du Nord. Bulletin de la Société entomologique de France 72: 20–25. [Google Scholar]
- de Lesse H. (1968) Formules chromosomiques de Lépidoptères Rhopalocères d´Uganda et du Kenya. Annales de la Societe Entomologique de France (NS) 4: 581–599. [Google Scholar]
- de Lesse H. (1970a) Les nombres de chromosomes chez les Lépidoptères Rhopalocères en Amérique centrale et Colombie. Annales de la Societe Entomologique de France (NS) 6: 347–358. [Google Scholar]
- de Lesse H. (1970b) Formules chromosomiques de quelques Lépidoptères Rhopalocères de Guyane. Annales de la Societe Entomologique de France (NS) 6: 849–855. [Google Scholar]
- de Lesse H. (1970c) Formules chromosomiques de quelques Rhopalocères paléarctiques [Lep.]. Bulletin de la Société entomologique de France 75: 214–218. [Google Scholar]
- de Lesse H. (1972) Nombres de chromosomes de quelques Lépidoptères Rhopalocères de Madagascar. Bulletin de la Société entomologique de France 77: 9–11. [Google Scholar]
- de Lesse H, Brown KS Jr. (1971) Formules chromosomiques de Lépidoptères Rhopalocères du Bresil. Bulletin de la Société entomologique de France 76: 131–137. [Google Scholar]
- de Lesse H, Condamin M. (1962) Formules chromosomiques de quelques Lépidoptères Rhopalocères du Sénégal. Bulletin de L’Institut Français d’Afrique Noire. Série A, Sciences Naturalles 24(2): 464–473. [Google Scholar]
- De Prins W, van der Poorten D. (1995) Rhopalocera and Grypocera of Turkey 14. Taxonomic revision of the Pyrgus alveus (Hübner, [1803]) complex from Greece to West China, with description of two new species from southern Turkey (Lepidoptera: Hesperiidae). Phegea 23(1): 1–44. [Google Scholar]
- Emmel TC, Eliazar PJ, Brown KS Jr, Suomalainen E. (1995) Chromosome evolution in the Papilionidae. In: Scriber JM, Tsubaki Y, Lederhouse RC. (Eds) Swallowtail butterflies: their ecology and evolution.Scientific Publishers, Gainesville, 283–298.
- Emmel TC, Trew HR. (1973) Chromosomes of skipper butterflies from Southwestern North-America (Lepidoptera, Hesperiidae). Cytologia 38(1): 45–53. doi: 10.1508/cytologia.38.45 [DOI] [PubMed] [Google Scholar]
- Federley H. (1938) Chromosomenzahlen finnländischer Lepidopteren. I. Rhopalocera. Hereditas 24: 397–464. doi: 10.1111/j.1601-5223.1938.tb03219.x [Google Scholar]
- Freeman HA. (1969) Systematic review of the Megathymidae. Journal of the Lepidopterist’s Society 23(Supplement 1): 1–59. [Google Scholar]
- Goodpasture C. (1976) High-resolution chromosome analysis in Lepidoptera. Annals of the Entomological Society of America 69(4): 764–771. [Google Scholar]
- Dinca V, Lukhtanov VA, Talavera G, Vila R. (2011) Unexpected layers of cryptic diversity in Wood White Leptidea butterflies. Nature Communications 2: 1-234. doi: 10.1038/ncomms1329 [DOI] [PubMed] [Google Scholar]
- Hesselbarth G, Van Oorschot H, Wagener S. (1995) Die Tagfalter der Türkei unter Berücksichtigung der angrenzenden Länder. Vol. 1-3. Bocholt, Selbstverlag S. Wagener, 1354 pp. [Google Scholar]
- ICZN (2000) Opinion 1944: Papilio sylvanus Esper, 1777 (currently known as Ochlodes sylvanus or O. venatus faunus; Insecta, Lepidoptera: specific name conserved. Bulletin of Zoological Nomenclature 57: 56–57. [Google Scholar]
- Jones RN, González-Sánchez M, González-García M, Vega JM, Puertas MJ. (2008) Chromosomes with a life of their own. Cytogenetic and Genome Research 120: 265–280. doi: 10.1159/000121076 [DOI] [PubMed] [Google Scholar]
- Kandul NP, Lukhtanov VA, Dantchenko AV, Coleman JWS, Sekercioglu CH, Haig D, Pierce NE. (2004) Phylogeny of Agrodiaetus Hübner 1822 (Lepidoptera: Lycaenidae) inferred from mtDNA sequences of COI and COII and nuclear sequences of EF1-α: Karyotype diversification and species radiation. Systematic Biology 53(2): 278–298. doi: 10.1080/10635150490423692 [DOI] [PubMed] [Google Scholar]
- Kandul NP, Lukhtanov VA, Pierce NE. (2007) Karyotypic diversity and speciation in Agrodiaetus butterflies. Evolution 61(3): 546–559. doi: 10.1111/j.1558-5646.2007.00046.x [DOI] [PubMed] [Google Scholar]
- King M. (1993) Species evolution. Cambridge, 336 pp. [Google Scholar]
- Kumagai Y, Abe A, Kudoh K. (2010) A survey of chromosome numbers of seven species of Hesperiidae in the neotropical region (Lepidoptera). Transactions of the Lepidopterological Society of Japan 61(1): 87–91. [Google Scholar]
- Larsen TB. (1975) Chromosome numbers and notes on testicular morphology of some Lebanese Rhopalocera (Insecta Lepidoptera). Entomologica Scandinavica 6(3/4): 253–260. doi: 10.1163/187631275X00091 [Google Scholar]
- Larsen TB. (1982) Gegenes pumilio Hoffmannsegg, 1804; a review with cytological evidence that two species are involved (Hesperiidae). Nota Lepidopterologica 5(2/3): 103–110. [Google Scholar]
- Lorković Z. (1941) Die Chromosomenzahlen in der Spermatogenese der Tagfalter. Chromosoma 2: 155–191. doi: 10.1007/BF00325958 [Google Scholar]
- Lorković Z. (1990) The butterfly chromosomes and their application in systematics and phylogeny. In: Kudrna O. (Ed.) Butterflies of Europe.Volume 2. Wiesbaden, Aula-Verlag, 332–396.
- Lukhtanov VA. (1991) Evolution of the karyotype and system of higher taxa of the Pieridae (Lepidoptera) of the world fauna. Entomologicheskoe Obozrenie 70(3): 619–641. [Google Scholar]
- Lukhtanov VA. (2000) Sex chromatin and sex chromosome systems in nonditrysian Lepidoptera (Insecta). Journal of Zoological Systematics and Evolutionary Research 38(2): 73–79. doi: 10.1046/j.1439-0469.2000.382130.x [Google Scholar]
- Lukhtanov VA, Dinca V, Talavera G, Vila R. (2011) Unprecedented within-species chromosome number cline in the Wood White butterfly Leptidea sinapis and its significance for karyotype evolution and speciation. BMC Evolutionary Biology 11: 109. doi: 10.1186/1471-2148-11-109 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lukhtanov VA, Kandul NP, Plotkin JB, Dantchenko AV, Haig D, Pierce NE. (2005) Reinforcement of pre-zygotic isolation and karyotype evolution in Agrodiaetus butterflies. Nature 436(7049): 385–389. doi: 10.1038/nature03704 [DOI] [PubMed] [Google Scholar]
- Lukhtanov VA, Shapoval NA, Dantchenko AV. (2008) Agrodiaetus shahkuhensis sp. n. (Lepidoptera, Lycaenidae), a cryptic species from Iran discovered by using molecular and chromosomal markers. Comparative Cytogenetics 2(2): 99–114. [Google Scholar]
- Lukhtanov VA, Vila R, Kandul NP. (2006) Rearrangement of the Agrodiaetus dolus species group (Lepidoptera, Lycaenidae) using a new cytological approach and molecular data. Insect Systematics and Evolution 37(3): 325–334. doi: 10.1163/187631206788838563 [Google Scholar]
- Maeki K. (1953) A chromosome study of Japanese butterflies. Kwansei Gakuin Iniversity Annual Studies 1: 67–70. [Google Scholar]
- Maeki K. (1961) Chromosome numbers of butterflies from North America. Zoological Magazine (Tokyo) 70: 165–169. [Google Scholar]
- Maeki K, Ae A. (1968a) A chromosome study of seventeen species of butterflies from Hong Kong (Lep. Rhopalocera). Kontyu 36(1): 65–74. [Google Scholar]
- Maeki K, Ae A. (1968b) Studies of the chromosomes of Formosan Rhopalocera. 1. Papilionidae and Hesperiidae. Kontyu 36(2): 116–123. [Google Scholar]
- Maeki K, Ae A. (1979) Chromosomal studies in interspecific hybrids of butterflies (Papilionidae, Lepidoptera). XV. Proceedings of the Japan Academy (B) 55: 295–299. [Google Scholar]
- Maeki K, Makino S. (1953) Chromosome numbers of some Japanese Rhopalocera. Lepidoptera News 7: 36–38. [Google Scholar]
- Maeki K, Ogata M. (1971) A chromosome study of eighteen species of butterflies from Australia (Lep. Rhopalocera). Kontyu 39(1): 1–8. [Google Scholar]
- Maeki K, Remington CL. (1960) Studies of the chromosomes of North American Rhopalocera 2. Hesperiidae, Megathymidae and Pieridae. The Journal of the Lepidopterists’ Society 14: 37–57. [Google Scholar]
- Przybyłowicz Ł, Lukhtanov V, Lachowska-Cierlik D. (2014) Towards the understanding of the origin of the Polish remote population of Polyommatus (Agrodiaetus) ripartii (Lepidoptera: Lycaenidae) based on karyology and molecular phylogeny. Journal of Zoological Systematics and Evolutionary Research 52(1): 44–51. doi: 10.1111/jzs.12040 [Google Scholar]
- Robinson R. (1971) Lepidoptera genetics. Pergamon Press, Oxford, 687 pp. [Google Scholar]
- Saitoh K. (1979) A note on the haploid karyotype of the Mediterranean skipper Gegenes nostrodamus (Lepidoptera, Hesperiidae) from Israel. Chromosome Information Service 27: 8–9. [Google Scholar]
- Saitoh K. (1982) Spermatocyte chromosomes of five taxa of Rhopalocera from Oman. Chromosome Information Service 33: 10–12. [Google Scholar]
- Saitoh K. (1984) Chromosomes of three butterfly taxa from Yemen. Tyo to Ga 34(4): 167–170. [Google Scholar]
- Saitoh K, Abe A. (1981) Chromosome numbers in twenty-four taxa of Rhopalocera from the People’s Republic of China. Chromosome Information Service 31: 18–19. [Google Scholar]
- Saitoh K, Kumagai Y. (1974) Notes on the spermatocyte chromosomes of four species of west Malaysian butterflies. Chromosome Information Service 16: 4–6. [Google Scholar]
- Saitoh K, Abe A, Kudoh K. (1978) Meiotic chromosomes of Choaspes benjaminii japonica (Lepidoptera, Hesperiidae). Chromosome Information Service 25: 28–29. [Google Scholar]
- Saitoh K, Kumagai Y, Abe A. (1991) Notes on the spermatocyte chromosomes of six taxa of Formosan butterflies. Tyo to Ga 42(2): 47−51. [Google Scholar]
- Saura A, von Schoultz B, Saura AO, Brown KS Jr. (2013) Chromosome evolution in Neotropical butterflies. Hereditas 150: 26–37. doi: 10.1111/j.1601-5223.2013.00008.x [DOI] [PubMed] [Google Scholar]
- Suomalainen E. (1969) Chromosome evolution in the Lepidoptera. Chromosomes Today 2: 132–138. [Google Scholar]
- Talavera G, Lukhtanov V, Rieppel L, Pierce NE, Vila R. (2013) In the shadow of phylogenetic uncertainty: the recent diversification of Lysandra butterflies through chromosomal change. Molecular Phylogenetics and Evolution 69: 469–478. doi: 10.1016/j.ympev.2013.08.004 [DOI] [PubMed] [Google Scholar]
- Vershinina AO, Lukhtanov VA. (2010) Geographical distribution of the cryptic species Agrodiaetus alcestis alcestis, A. alcestis karacetinae and A. demavendi (Lepidoptera, Lycaenidae) revealed by cytogenetic analysis. Comparative Cytogenetics 4(1): 1–11. doi: 10.3897/compcytogen.v4i1.21 [Google Scholar]
- Vershinina AO, Lukhtanova VA. (2013) Dynamics of chromosome number evolution in the Agrodiaetus phyllis species complex (Insecta: Lepidoptera). Cell and Tissue Biology 7(4): 379–381. doi: 10.1134/S1990519X13040159 [PubMed] [Google Scholar]
- Vila R, Lukhtanov VA, Talavera G, Gil-T F, Pierce NE. (2010) How common are dot-like distribution ranges? Taxonomical oversplitting in Western European Agrodiaetus (Lepidoptera, Lycaenidae) revealed by chromosomal and molecular markers. Biological Journal of the Linnean Society 101: 130–154. doi: 10.1111/j.1095-8312.2010.01481.x [Google Scholar]
- Warren AD, Ogawa J, Brower AVZ. (2008) Phylogenetic relationships of subfamilies and circumscription of tribes in the family Hesperiidae (Lepidoptera: Hesperioidea). Cladistics 24: 642–676. doi: 10.1111/j.1096-0031.2008.00218.x [Google Scholar]
- Warren AD, Ogawa JR, Brower AVZ. (2009) Revised classification of the family Hesperiidae (Lepidoptera: Hesperioidea) based on combined molecular and morphological data. Systematic Entomology 34(3): 467–523. doi: 10.1111/j.1365-3113.2008.00463.x [Google Scholar]
- Wesley DJ, Emmel TC. (1975) The chromosomes of Neotropical butterflies from Trinidad and Tobago. Biotropica 7: 24–31. doi: 10.2307/2989796 [Google Scholar]
- White MJD. (1973) Animal cytology and evolution. Cambridge, 961 pp. [Google Scholar]