Maternal Care under Large Clutches with Small Eggs: The Evolution of Life History Traits in Shield Bugs.

AbstractPatterns in the correlated evolution of parental care and life history traits are long established but controversial. Although parental care is related to large egg size in many taxa, conflicting results have also been reported. To test the evolutionary relationships between parental care and life history traits, we performed phylogenetic comparative analyses using shield bugs (Heteroptera: Acanthosomatidae), in which maternal guarding of eggs and young has repeatedly evolved. Our analyses revealed that female body size affected reproductive resource allocation. Contrary to the expectations of current theories, the acquisition of maternal care was associated with small eggs, large clutches, and large egg resource allocation. There was a greater trade-off between egg size and clutch size in caring species than in noncaring species. Egg and hatchling developmental rates were not correlated with egg size but were slower in caring species than in noncaring species. Analyses of evolutionary transitions suggest that the establishment of large clutches, small eggs, and large egg resource allocation preceded the evolution of maternal care. To our knowledge, this is the first study clarifying the evolution of parental care linked with small eggs in invertebrates.

Morphology of the pterothoracic musculature in Paraneoptera and its phylogenetic implication (Insecta: Neoptera).

Although the monophyly of Paraneoptera (=hemipteroid orders or Acercaria, composed of Psocodea, Thysanoptera and Hemiptera) has been widely accepted morphologically, the results from molecular phylogenetic and phylogenomic analyses contradict this hypothesis. In particular, phylogenomic analyses provide strong bootstrap support for the sister group relationship between Psocodea and Holometabola, that is, paraphyly of Paraneoptera. Here, we examined the pterothoracic musculature of Paraneoptera, as well as a wide range of other neopterous insect orders, and analysed its phylogenetic implication. By using the synchrotron microcomputed tomography (µCT) and parsimony-based ancestral state reconstruction, several apomorphic conditions suggesting the monophyly of Paraneoptera, such as the absence of the II/IIItpm7, IIscm3, IIIspm2 and IIIscm3 muscles, were identified. In contrast, no characters supporting Psocodea + Holometabola were recovered from the thoracic muscles. These results provide additional support for the monophyly of Paraneoptera, together with the previously detected morphological apomorphies of the head, wing base, and abdomen.

Two new species of Cameraria Chapman (Lepidoptera: Gracillariidae) associated with Salix or Cornus in Japan.

Two new species of the genus Cameraria Chapman, 1902, Cameraria riparia sp. nov. and Cameraria corni sp. nov., are described from Japan. Larval setal maps, illustrations and/or photographs of wing patterns, wing venations and genitalia are provided for both species, and the systematic positions of the two species are discussed based on their morphologies. The larvae of C. riparia feed on Salix spp. and make blotch mines, whereas C. corni larvae feed on Cornus kousa subsp. kousa and make linear blotch mines. C. riparia was collected on Hokkaido and Honshu Islands, and considerable differences in the male genital characters were detected between the two populations. However, a molecular phylogenetic analysis based on the COI barcode region indicated that there was no clear genetic differentiation between the two populations (maximum divergence, 1.41%). C. corni was collected on Honshu and Kyushu Islands, and this is the first record of the trophic association of Lithocolletinae with Cornaceae.

Are males just passive? Coupling mechanism of the Brazilian cave insects with inverted genitalia.

Species of the Brazilian cave barklouse genus Neotrogla (Psocodea: "Psocoptera": Trogiomorpha: Prionoglarididae: Sensitibillini) are known to have a "female penis (gynosome)" that functions as an intromittent organ inserted into the membranous pouches in the simple male genital chamber during copulation to receive semen. However, the functions of other male and female genital structures and the copulatory processes of Neotrogla were completely unknown to date. Based on µCT observation of the male and female postabdomen and connected muscles both before and in copula, we clarified the functions of the male and female genital structures. In addition, based on the analyses of the established 3D models, we concluded that precise and rigid contact of multiple genital structures, and step-by-step releases of each holding mechanism achieved by the cooperation of both sexes are involved in the copulatory processes. The coevolution between the male and female genital structures in Neotrogla may provide a new example for the evolution of tolerance traits.

Acquisition of novel muscles enabled protruding and retracting mechanisms of female penis in sex-role reversed cave insects.

Brazilian sex-role reversed cave insects (genus Neotrogla) have a striking structure called the gynosome (or female penis), which deeply penetrates male vagina-like genitalia during copulation to receive nutritious semen. However, the protruding and retracting mechanisms of the female penis, including their evolutionary origin, are poorly understood. By using micro-computed tomography (µCT), we compared the genital morphology and musculature between species with a gynosome and others lacking this structure. As a result, we discovered two groups of muscles related to the protrusion and retraction of gynosomes. These muscles were also observed in species with non-protrusible prepenis. This suggests that evolution of these muscles preceded the acquisition of the protruding function of the gynosome, originally having a putative stimulatory function to receive nutritious semen. This intermediate stage probably allowed for the reversal of genital functions.

Morphology and phylogenetic significance of the thoracic muscles in Psocodea (Insecta: Paraneoptera).

The thoracic musculature of the insect order Psocodea has been examined in only a few species of a single suborder to date. In the present study, we examined the thoracic musculature of species selected from all three suborders of Psocodea to elucidate the ground plan of the order and to examine the phylogenetic utility of the character system. The sister-group relationship between the suborders Troctomorpha and Psocomorpha received support from two novel nonhomoplasious synapomorphies, although the support from other morphological characters for this relationship is ambiguous. The sister-group relationship between the infraorders Epipsocetae and Psocetae also received support from one nonhomoplasious synapomorphy, although no other morphological characters supporting this relationship have been identified to date. The present examination revealed the potential of thoracic muscle characters for estimating deep phylogeny, possibly including interordinal relationships.

Exploration of the homology among the muscles associated with the female genitalia of the three suborders of Psocodea (Insecta).

By using µCT technology, we reconstructed 3D models of the female genital structures and associated muscles of seven species from three suborders of Psocodea (free-living species only, formerly known as independent insect order "Psocoptera"). The homology of the female genital structures and associated muscles of different species is discussed. A total of 21 muscle groups were observed, and except for one muscle, all were homologized throughout the order. Moreover, some of the homologous muscles could be identified confidently in holometabolan insects. Using the muscles as landmarks, we discuss the homology of the ovipositor valves between Psocodea and other neopteran insects. Most importantly, the ovipositor of the suborder Trogiomorpha was identified to consist of the well-developed external valve (V3) plus a remnant of the dorsal valve (V2). We also examined the phylogenetic information included in the female genital muscles and found that certain muscles provide useful information and support deeper nodes (e.g., monophyly of the suborder Psocomorpha). The present study of female genital muscles not only helps us to better understand the phylogeny of Psocodea but also provides a solid foundation for research on muscle evolution.

Evolution of nuptial gifts and its coevolutionary dynamics with male-like persistence traits of females for multiple mating.

BACKGROUND: Many male animals donate nutritive materials during courtship or mating to their female mates. Donation of large-sized gifts, though costly to prepare, can result in increased sperm transfer during mating and delayed remating of the females, resulting in higher paternity. Nuptial gifting sometimes causes severe female-female competition for obtaining gifts (i.e., sex-role reversal in mate competition) and selection on females to increase their mating rate, changing the intensity of sperm competition and the resultant paternity gains. We built a theoretical model to simulate such coevolutionary feedbacks between nuptial gift size (male trait) and propensity for multiple mating (female trait). Donation of nuptial gifts sometimes causes development of female persistence trait for gift acquisition. We also analyzed the causes and consequences of this type of traits, taking double receptacles for nutritious seminal gifts, which are known to occur in an insect group with a "female penis" (Neotrogla spp.), as an illustrative example. RESULTS: Our individual-based simulations demonstrated that female-female competition for male-derived nutrients always occur when the environment is oligotrophic and mating costs are low for females. However, a positive correlation between donated gift size and the resultant paternity gain was a requisite for the co-occurrence of large gifts and females' competitive multiple mating for the gifts. When gift donation satisfied female demands and thus resulted in monandry, exaggeration of nuptial gift size also occurred under the assumption that the last male monopolizes paternity. The evolution of double slots for gift acquisition and digestion (female persistence trait) always occurred when males could not satisfy the demands of females for gifts. However, through coevolutionary reduction in male gift size, fixation of this trait in a population drastically reduced the average female fitness. CONCLUSION: Sperm usage patterns, which have rarely been examined for animals with nuptial gifts, can be a critical factor for determining the extent of exaggeration in nuptial gifting. Sex-role reversals in mate competition, as a result of donation of nuptial gifts from males to females, can involve the evolution of male-like, persistent traits in females that reduce population productivity, as is the case with persistence traits in males.

The first record of Caenis rivulorum (Ephemeroptera: Caenidae) from Japan.

BACKGROUND: Caenis rivulorum Eaton, 1884 is widely distributed and has been reported from a wide range in the Palearctic Region. NEW INFORMATION: We report this species from Japan for the first time, from five localities of Hokkaido, based on morphology and molecular data.

Phylogenomics of Parasitic and Nonparasitic Lice (Insecta: Psocodea): Combining Sequence Data and Exploring Compositional Bias Solutions in Next Generation Data Sets.

The insect order Psocodea is a diverse lineage comprising both parasitic (Phthiraptera) and nonparasitic members (Psocoptera). The extreme age and ecological diversity of the group may be associated with major genomic changes, such as base compositional biases expected to affect phylogenetic inference. Divergent morphology between parasitic and nonparasitic members has also obscured the origins of parasitism within the order. We conducted a phylogenomic analysis on the order Psocodea utilizing both transcriptome and genome sequencing to obtain a data set of 2370 orthologous genes. All phylogenomic analyses, including both concatenated and coalescent methods suggest a single origin of parasitism within the order Psocodea, resolving conflicting results from previous studies. This phylogeny allows us to propose a stable ordinal level classification scheme that retains significant taxonomic names present in historical scientific literature and reflects the evolution of the group as a whole. A dating analysis, with internal nodes calibrated by fossil evidence, suggests an origin of parasitism that predates the K-Pg boundary. Nucleotide compositional biases are detected in third and first codon positions and result in the anomalous placement of the Amphientometae as sister to Psocomorpha when all nucleotide sites are analyzed. Likelihood-mapping and quartet sampling methods demonstrate that base compositional biases can also have an effect on quartet-based methods.[Illumina; Phthiraptera; Psocoptera; quartet sampling; recoding methods.].

A revision of Strigiphilus (Insecta: Phthiraptera: Philopteridae) from Japan.

The Japanese species of the genus Strigiphilus Mjöberg, 1910 (Insecta: Phthiraptera: Philopteridae) are revised. Six species are recorded, including a new species belonging to the cursitans species-group: Strigiphilus stenocephalus new species, described from the type host Otus bakkamoena semitorques and based on specimens originally identified and reported by Uchida (1949) as Strigiphilus rostratus (Burmeister, 1838). A lectotype for Strigiphilus laticephalus (Uchida, 1949) (type host: Strix aluco yamadae) is designated and redescribed, and this louse species is synonymized under Strigiphilus cursor (Burmeister, 1838). Strigiphilus ceblebrachys (Denny, 1842), S. heterogenitalis Emerson Elbel, 1957 and S. tuleskovi Balát, 1958 are recorded for the first time in Japan. Also, Strix uralensis and Otus sunia japonicus are recorded as new hosts for Strigiphilus heterogenitalis and S. tuleskovi respectively.

New records of chewing lice (Phthiraptera: Amblycera, Ischnocera) from the black-faced spoonbill (Platalea minor).

Three species of chewing lice-Eucolpocephalum femorale (Piaget, 1880) (Amblycera: Menoponidae), Ibidoecus plataleae (Denny, 1842) (Ischnocera: Philopteridae) and Ardeicola plataleae (Linnaeus, 1758) (Ischnocera: Philopteridae)-are reported from the black-faced spoonbill (Platalea minor Temminck Schlegel, 1849) in Japan. These three louse species are new records for this host. The black-faced spoonbill is classified as a "Critically Endangered" species in the IUCN Red List; although its species of lice are known to infest other species of spoonbills, these lice are endangered at the population level.

Why Did a Female Penis Evolve in a Small Group of Cave Insects?

The evolution of a female penis is an extremely rare event and is only known to have occurred in a tribe of small cave insects, Sensitibillini (Psocodea: Trogiomorpha: Prionoglarididae). The female penis, which is protrudable and inserted into the male vagina-like cavity during copulation to receive semen, is thought to have evolved independently twice in this tribe, in the Brazilian Neotrogla and the African Afrotrogla. These findings strongly suggest that there are some factors unique to Sensitibillini that have facilitated female penis evolution. Here, several hypothetical factors are presented that may have enabled the evolution of the female penis in Sensitibillini. The female-female competition for nutritious semen, the oligotrophic environment, and the twin insemination slots with switching valve are considered to be the driving factors for female penis evolution. Additionally, the following factors are considered responsible for relaxing the constraint against female penis evolution: preexistence of the female-above mating position, the elongated duct connecting the female pre-penis with the sperm storage organ, and the small male genital cavity accepting the female genital tubercle bearing the opening of this duct. Understanding the factors enabling female penis evolution may also shed light on the evolution of the male penis.

Functional morphology of Trichadenotecnum male and female genitalia analyzed using µCT (Insecta: Psocodea: Psocomorpha).

Although the great genital diversity of the barklouse genus Trichadenotecnum has been described in previous studies, the specific function of the genital structures during the copulation process has received less investigative attention. We reconstructed 3D-models of each structure of the male and female genitalia of Trichadenotecnum incognitum in copula and those of uncopulated male and female of Trichadenotecnum pseudomedium. By comparing the changes in male and female genital structures and related muscles in copulated and uncopulated states, the function of each genital structure can be described. During the copulation, we found that the female subgenital plate was hooked into the male body by the distal process on the male paraproct and was fixed by the male epiproct, hypandrium and phallosome. In addition, sexual coevolution was suggested by tightly contacting structures, that is, thorny male hypandrium and thickened membrane around the female spermapore plate. These results not only give us a new understanding copulation process of Trichadenotecnum, but also explain the reasons why genital structures are so divers in the genus.

Independent origins of female penis and its coevolution with male vagina in cave insects (Psocodea: Prionoglarididae).

The cave-dwelling psocid tribe Sensitibillini (Afrotrogla, Neotrogla and Sensitibilla) is of special morphological and evolutionary interest because of its possession of reversed copulatory organs: i.e. females of Afrotrogla and Neotrogla have a penis-like organ. The female penis structure is highly variable among taxa, as is the case of the male penis in animals with normal copulatory organs. Here, we present the first molecular phylogeny of Sensitibillini and analyse the evolutionary pattern of their genitalia. Afrotrogla and Neotrogla did not form a monophyletic clade, and their female penis structures are significantly different, suggesting two independent origins of the female penis within Sensitibillini. In Neotrogla, the species that has a simple female penis is embedded among species that have an elaborate penis, and detailed structures of the female penis elaborations are in exact agreement among species, suggesting a secondary simplification of the female penis. A correlated evolutionary pattern between male and female genitalia was also detected. This coevolution of genitalia may suggest that sexual conflict or cryptic 'male' choice drove the diversity of the female penis, as is the case of male penile diversity in animals with conventional genitalia.

Phylogenomics and the evolution of hemipteroid insects.

Hemipteroid insects (Paraneoptera), with over 10% of all known insect diversity, are a major component of terrestrial and aquatic ecosystems. Previous phylogenetic analyses have not consistently resolved the relationships among major hemipteroid lineages. We provide maximum likelihood-based phylogenomic analyses of a taxonomically comprehensive dataset comprising sequences of 2,395 single-copy, protein-coding genes for 193 samples of hemipteroid insects and outgroups. These analyses yield a well-supported phylogeny for hemipteroid insects. Monophyly of each of the three hemipteroid orders (Psocodea, Thysanoptera, and Hemiptera) is strongly supported, as are most relationships among suborders and families. Thysanoptera (thrips) is strongly supported as sister to Hemiptera. However, as in a recent large-scale analysis sampling all insect orders, trees from our data matrices support Psocodea (bark lice and parasitic lice) as the sister group to the holometabolous insects (those with complete metamorphosis). In contrast, four-cluster likelihood mapping of these data does not support this result. A molecular dating analysis using 23 fossil calibration points suggests hemipteroid insects began diversifying before the Carboniferous, over 365 million years ago. We also explore implications for understanding the timing of diversification, the evolution of morphological traits, and the evolution of mitochondrial genome organization. These results provide a phylogenetic framework for future studies of the group.

A biological switching valve evolved in the female of a sex-role reversed cave insect to receive multiple seminal packages.

We report a functional switching valve within the female genitalia of the Brazilian cave insect Neotrogla. The valve complex is composed of two plate-like sclerites, a closure element, and in-and-outflow canals. Females have a penis-like intromittent organ to coercively anchor males and obtain voluminous semen. The semen is packed in a capsule, whose formation is initiated by seminal injection. It is not only used for fertilization but also consumed by the female as nutrition. The valve complex has two slots for insemination so that Neotrogla can continue mating while the first slot is occupied. In conjunction with the female penis, this switching valve is a morphological novelty enabling females to compete for seminal gifts in their nutrient-poor cave habitats through long copulation times and multiple seminal injections. The evolution of this switching valve may have been a prerequisite for the reversal of the intromittent organ in Neotrogla.

Structure and evolution of the stigmapophysis-A unique repose wing-coupling structure in Psocodea.

The gain of foldable wings is regarded as one of the key innovations enabling the present-day diversity of neopteran insects. Wing folding allows compact housing of the wings and shields the insect body from damage. Wing-fixing systems have evolved in some insects, probably to increase the durability of the shielding function by the wings. Bark lice (Psocodea) are known to possess a unique wing-to-wing repose coupling system, but a detailed morphological and evolutionary study of this system is lacking. In this study, we examined this repose coupling structure by SEM in 32 species including representatives of all three suborders of bark lice (Trogiomorpha, Troctomorpha and Psocomorpha). We concluded that the repose wing-coupling apparatus independently evolved twice within Psocodea. In Trogiomorpha, the apparatus is located on the subcostal vein of the forewing and is composed of elongated rib-like structures. In Troctomorpha and Psocomorpha, in contrast, the repose coupling structure is located on the radius vein of the forewing and is formed by a swollen vein. These morphological and developmental differences in the repose coupling structures also provide phylogenetic information at different systematic levels.

Morphology of the elytral base sclerites.

The elytral base sclerites (= sclerites located at the articular region between the forewing and thorax in Coleoptera) of selected taxa were examined and homologized. Although the elytral base sclerites are highly modified compared to the wing base sclerites of the other neopterans, they can be homologized by using the conservative wing flapping and folding lines as landmarks. A reduction of the first axillary sclerite was identified as a general trend of the elytral base sclerites, although the sclerite usually has a very important function to mediate flight power from the notum to the wing. This result indicates that the functional constraint against the basal sclerites is relaxed because of the lack of an ability to produce flight power by elytra. In contrast, the elytral folding system formed by the basal sclerites is well retained, which probably occurs because proper wing folding is a key for the shelter function of the elytra. The elytral base sclerites apparently contain more homoplasies than the serially homologous hindwing base sclerites of Coleoptera, which suggests that the structure is less useful for higher-level systematics. However, the faster evolutionary rate of the elytral base sclerites suggests there is potential for studying the lower-level phylogeny of Coleoptera.