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Comparative analysis reveals the complex role of histoblast nest size in the evolution of novel insect abdominal appendages in Sepsidae (Diptera) - PubMed

  • ️Mon Jan 01 2018

Comparative Study

Comparative analysis reveals the complex role of histoblast nest size in the evolution of novel insect abdominal appendages in Sepsidae (Diptera)

Dacotah Melicher et al. BMC Evol Biol. 2018.

Abstract

Background: The males of some sepsid species (Sepsidae: Diptera) have abdominal appendages that are remarkable in several ways. They are sexually dimorphic, have a complex evolutionary history of gain and loss, and can be jointed and thus highly mobile. The sternite brushes are used extensively in complex courtship behaviors that differ considerably between species and during mating. The abdominal appendages have a novel developmental pathway developing from histoblast nests rather than imaginal discs.

Results: We focus on the evolution of cell number, nest area, and segment length in both sexes to understand how this tissue relates to the formation of novel abdominal appendages. We map histoblast nest size of wandering-phase larvae of 17 species across 10 genera to a phylogenetic tree of Sepsidae and demonstrate that abdominal appendages require significant increases of histoblast nest size and cell number in most species while one species produces small appendages even without such modifications. In species with particularly large appendages, not only the nests on the fourth, but nests in neighboring segments are enlarged (Themira biloba, Themira putris). The loss of abdominal appendages corresponds to the loss of an enlarged fourth histoblast nest, although one species showed an exception to this pattern. One species that constitutes an independent origin of abdominal appendages (Perochaeta dikowi) uses an unusual developmental mechanism in that the histoblast nest sizes are not sexually dimorphic.

Conclusions: The surprisingly high diversity in histoblast size and degree of sexual dimorphism suggests that the developmental mechanism used for abdominal appendage formation in sepsids is highly adaptable. The presence of appendages usually correlate with increased histoblast cell number and in most cases appendage loss results in a return to ancestral histoblast morphology. However, we also identify several exceptions that indicate the abdominal appendages have a malleable developmental origin that is responsive to selection.

Keywords: Comparative morphology; Evolutionary history; Histoblast; Novelty; Sepsidae.

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Figures

Fig. 1
Fig. 1

Phylogeny of sepsid species with evolutionary history of gains and losses. The current phylogeny of Sepsidae supports one gain of the appendage and multiple losses. The species sampled for histoblast analysis represent one primary gain and three independent losses of the abdominal appendage as well as Orygma luctuosum, a sister group to the remaining sepsid species which lacks abdominal appendages. The pattern of gains and losses was inferred from a phylogeny with more taxa [18]

Fig. 2
Fig. 2

Abdominal view of adult flies of the sampled species. Species that posess the appendage are in green and species without appendages in red with independent losses indicated by number. Primary gain of the appendage (a, f, i-n) results in a modified sternite, joint and bristles as compared to the ancestral state (o). The current phylogeny supports three independent losses of the appendage (L1 = b-e, L2 = g, L3 = h). The degree of sternite modification and size of the appendages are highly variable between species. T. biloba and T. putris (k, l) posses extensive sternite modification and long appendage brushes relative to other species. Loss of the appendage also results in the loss of the modified sternite which returns to the ancestral state. Scale bars indicate 1 mm

Fig. 3
Fig. 3

Themira biloba larval epidermis (a) with ventral histoblast nests in abdominal segments enlarged showing a sexually dimorphic increase in nest size, cell number, and cell density peaking in the 4th abdominal segment (b-h). The 4th female histoblast nest is not significantly larger than nests in other segments and is shown for comparison (i). Scale bars indicate 500 μm (a) and 25 μm (b-i)

Fig. 4
Fig. 4

The histoblast nest in O. luctuosum shows no significant sexual dimorphism or increase in cell number or nest density in the 4th segment which likely represents the ancestral state. Refer to Table 3 for the number of individuals sampled

Fig. 5
Fig. 5

Primary gain of the appendage results in a strong sexual dimorphism and increase in cell number, nest size, and cell density within the nest in males peaking in the 4th abdominal segment which produces the abdominal appendage. Neighboring segments also show enlarged histoblast nests despite lacking the appendage. Females, which lack the appendage, show no significant difference in cell number or nest size between segments. Refer to Table 3 for the number of individuals sampled for each species

Fig. 6
Fig. 6

M. armillata and P. dikowi represent species with unusual histoblast nest patterns. Both possess the appendage, but nest morphology is not sexually dimorphic. P. dikowi females present the male phenotype having significantly enlarged nests in both sexes. M. armillata males present the female phenotype with no increase in nest size. M. armillata possesses diminished appendages and little sternite modification, indicating that small appendages do not require an increase in histoblast nest size. Refer to Table 3 for the number of individuals sampled for each species

Fig. 7
Fig. 7

Secondary loss of the abdominal appendage results in a loss of sexual dimorphism. Nest size across segments remains significantly different but no consistent pattern exists between species. This group includes three independent losses with A. indica, Dicranosepsis sp., S. latiforceps, and S. punctum representing L1, A. armata representing L2, and M. alberquerquei representing L3. Refer to Table 3 for the number of individuals sampled for each species

Fig. 8
Fig. 8

Phylogeny of sampled species indicating the degree of sexual dimorphism in histoblast cell number. Color of the terminal nodes indicates the ratio of male to female cell counts in the 4th segment histoblast nest with cooler colors indicating sexually dimorphic species. The value of the male:female ratio is reported. Colored boxes indicate whether the species has abdominal appendages (green) or does not (red). Independent losses are indicated as L1 – L3

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