Pseudomallada, Tsukaguchi, 1995

THE FOUR PSEUDOMALLADA View in CoL GROUPS

Aspöck et al. (2001) considered the species-rich genus Pseudomallada (then Dichochrysa ) in need of revision and suspected that it was not a monophyletic genus. Now we have evidence that the genus is monophyletic. Additionally, both molecular data and genital morphology support the same four distinct morphological species-groups within the genus. In only three cases, molecular analyses revealed singletons as sister taxa of molecular clades. In two of those, the shape of the gonapsis leans towards one of the four morphological groups. Thus, there are very few mismatches between molecularly determined clades and morphologically based gonapsis groups.

In most of the four species-groups, species distributions permit speculation on origins of the groups. The molecularly well-supported P1 clade most likely originated in Asia ( P. astur , P. alcestes , P. sp. 1 and P. sp. 2, P. cognatellus , P. parabolus , P. formosanus , P. ussuriensis ), with two independent range extensions into the Indian Ocean and Africa. Apertochrysa eurydera is present on most islands east of Africa and in eastern and northwestern parts of continental Africa. A small clade that includes the widespread species, P. sjostedti , also extends to the Mascarene Islands ( P. duplicatus ) and into southern Africa ( P. pulchrinus ).

The easily delineated prasinus -group (P3, G2) occurs mainly in Eurasia and northern Africa. Some of the species are difficult to identify reliably, especially the females. This might be the reason for the species names prasinus and abdominalis occurring several times on the list in Figure 1 View Figure 1 . We suspect that the prasinus -group comprises several undescribed cryptic species. In fact, Aspöck et al. (1980) reported that in large parts of northern Europe, P. prasinus and P. ventralis form mixed phenotypes. Additionally, the present study shows that except for P. benedictae , the species in the prasinus -group have similar DNA sequences for the three nuclear genes (P -distances are less than 0.009; Table 4). Indeed, sequences for all three genes were nearly the same in Swiss P. prasinus and P. abdominalis , while Greek P. prasinus and Italian P. abdominalis had ATPase sequences identical to each other. We could not identify cryptic species within the prasinus -group. However, P. marianus is the only species within the prasinus -group to deposit its eggs in bundles, possibly confirming its validity as a separate, cryptic species ( Duelli, 1994).

The flavifrons -group (part of P4, G3) is mainly African [ P. hamatus , P. myassalandicus , P. handschini , P. chloris , P. spissinervis , P. sp. gray from South Africa, P. luaboensis , P. gunvorae , P. kibonotoensis , and P. baronissus (recently synonymized, probably prematurely, with P. kibonotoensis )]. However, one small, well-supported molecular clade has colonized North America ( P. perfectus , P. macleodi , P. luctuosus ), while another small clade, which includes the widespread over averaged P. abdominalis ( Italy) – – – – – – – –

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site per substitutions P marianus . – – – – – – – 0.004 0.007

base of number P

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estimated as

prasinus . P ( Switzerland – – – – – 0.001 0.006 0.003 0.006

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clade

P

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ventralis

group P. – – – – 0.007 0.006 0.008 0.006 0.007

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prasinus prasinus

. Japan)

Pseudomallada P zelleri P. (– – – – 0.009 – 0.007 0.012 0.008 0.006 0.006 0.007 0.012 0.008 0.008 0.005 0.007 0.008

of taxa among taxa benedictae P. – 0.009 0.015 0.012 0.009 0.009 0.013 0.010 0.011

divergences the)).

Evolutionary between pairs

(

) Japan

(

Switzerland Switzerland ( Italy) () Greece

(shown are distances P

-. 4 Table sequence all. P benedictae . P zelleri . P prasinus P ventralis . P prasinus . P abdominalis .. P marianus . abdominalis P P. prasinus Uncorrected species P. flavifrons , extends across Europe ( P. ibericus , P. picteti ) and into Asia ( P. flavifrons ).

The venosus -group (P5, G4) may have its origin around the Mediterranean Sea [ P. clathratus , P. genei , P. venosus (also in western Asia)], but one cluster of species extends into Africa (the widespread P. nicolainus , the undescribed P. sp. Sodere from Ethiopia) and even as far as South Africa ( P. karooensis , P. rubicundus , P. tactus ).

There are only a few singletons between the molecular clades:

Apertochrysa edwardsi View in CoL is an Australian species. It clearly belongs to Pseudomallada View in CoL based on molecular data, but it has no tignum. Therefore, it had been placed in the genus Apertochrysa View in CoL , which Brooks & Barnard (1990) reported as having a small, T-shaped gonapsis but no tignum. Apertochrysa eurydera View in CoL similarly lacks a tignum but appears to be a member of the P1 molecular clade. It is clear that at least A. eurydera View in CoL , and probably A. edwardsi View in CoL , should be moved into Pseudomallada View in CoL s.s., based on molecular data and the shape of the gonapsis. In fact, the gonapsis of A. edwardsi View in CoL is very similar to that of P. alcestes View in CoL and P. sjostedti View in CoL . However, the gonapsis of A. eurydera View in CoL , which is allied on molecular grounds with the alcestes View in CoL -group, instead more closely resembles that of the flavifrons View in CoL -group, or even that of P. inopinatus View in CoL . In any case, our results suggest that the tignum is not definitive for the genus Pseudomallada View in CoL , even though both structures are present in all species of Pseudomallada View in CoL s.s. that we examined. Tsukaguchi’s report of no gonapsis in Apertochrysa View in CoL is probably in error, likely caused by accidental substitution of the word gonapsis for tignum on page 18 of his monograph ( Tsukaguchi, 1995).

Three species of the genus Apertochrysa View in CoL ( A. albolineatoides Tsukaguchi View in CoL , A. eurydera View in CoL , and A. edwardsi View in CoL ) are presently scattered across the phylogenetic tree of the Chrysopidae View in CoL ( Fig. 1 View Figure 1 ; Supporting Information, Figs S1 View Figure 1 and S 2 View Figure 2 ; Haruyama et al., 2008). Apertochrysa albolineatoides View in CoL appears within a clade that includes Cunctochrysa Hölzel View in CoL and Meleoma Fitch ( Haruyama et al., 2008) View in CoL , while we have shown here the likelihood that A. eurydera View in CoL and A. edwardsi View in CoL are part of Pseudomallada View in CoL s.l. ( Fig. 1 View Figure 1 ). These results indicate that a comprehensive systematic revision of Apertochrysa View in CoL is necessary (A. Mochizuki et al., in preparation).

Another singleton is P. inornatus , shown in Figure 1 View Figure 1 as molecularly distinct from and the sister taxon to P2. The shape of its tiny gonapsis ( Fig. 4B View Figure 4 ) is markedly different from that characterizing any other Pseudomallada species. Pseudomallada inornatus is known from Europe and the Caucasus.

Pseudomallada inopinatus , a rare endemic highland species on the island of La Réunion east of Madagascar, belongs to the species-rich clade P4, comprising mainly African species. It appears on the tree as an isolated sister taxon to clade P5. Its gonapsis ( Fig. 4C View Figure 4 ), however, is unlike others in P5. The most similar gonapsis to that of P. inopinatus is found in species such as P. kibonotoensis , which belong to G4 but are still part of the P4 clade.

ADAPTIVE COLORATION AND OVIPOSITION

Not all ‘green lacewings’ are green. Some even change their body coloration during the adult’s lifetime (Duelli, Johnson, et al., 2014). Variations in body coloration reflect cryptic adaptations to environmental conditions. A well-known characteristic of the genus Pseudomallada is the difference in body coloration among closely related species. From Figure 1 View Figure 1 it is clear that in two groups (G1 and G2), all species are green, whereas in clade P4 (G3 and G4), some but not all species are grey or brown. These non-green species occur in different sub-clades, interspersed phylogenetically with green species. The conclusion is that green must have been the original body colour in Pseudomallada . Grey or brown body coloration, always linked with white or greyish eggs, and often with bundled egg pedicels, is a derived trait, developed independently in dry and hot habitats, where the vegetation is yellow, grey, or brown for most of the period when the adults are active. Even in a bluish-brownish species considered as green here ( P. clathratus ), a yellow mutation occurs in the wild in dry areas ( Duelli, 1994). In Europe, brownish-grey species such as P. venosus , P. genei , or P. venustus live only in the driest parts of the continent. Convergent evolution of grey or brown species in different genetic clusters leads to species that look very similar but have completely different shapes of their gonapses.

Not only the colour of the body and eggs is scattered among the phylogenetic clades but also the mode of egg deposition is polyphyletic. Clustered egg pedicels are particularly common in non-green lacewings, but they also occur in some green species in all groups. Depositing eggs singly or in bundles significantly influences the intensity of cannibalism ( Duelli & Johnson, 1992) and can be viewed as an adaptive trait ( Duelli, 1981). In a habitat with sufficient food for most larvae, depositing eggs singly is a more successful way to produce offspring. With scarce food, isolated tiny larvae soon starve to death, while larvae from bundled eggs have a chance to encounter sibling larvae, which can be attacked and eaten. Laboratory experiments have shown that with scarce food, at least one larva out of a daily bundle of about 20 eggs will survive to the adult stage ( Duelli & Johnson, 1992). From the distribution within the clusters in Figure 1 View Figure 1 of species with egg bundles, we cannot see an obvious link to particular habitat qualities, other than the observation that bundled eggs are more often deposited in species living in hot and dry climates. However, several green species living in rather lush habitat ( P. astur , P. marianus , and the North American species) show that there must be other reasons than climate for egg bundles.