Parasite escape mechanisms drive morphological diversification in avian lice

Abstract

Organisms that have repeatedly evolved similar morphologies owing to the same selective pressures provide excellent cases in which to examine specific morphological changes and their relevance to the ecology and evolution of taxa. Hosts of permanent parasites act as an independent evolutionary experiment, as parasites on these hosts are thought to be undergoing similar selective pressures. Parasitic feather lice have repeatedly diversified into convergent ecomorphs in different microhabitats on their avian hosts. We quantified specific morphological characters to determine (i) which traits are associated with each ecomorph, (ii) the quantitative differences between these ecomorphs, and (iii) if there is evidence of displacement among co-occurring lice as might be expected under louse-louse competition on the host. We used nano-computed tomography scan data of 89 specimens, belonging to four repeatedly evolved ecomorphs, to examine their mandibular muscle volume, limb length and three-dimensional head shape data. Here, we find evidence that lice repeatedly evolve similar morphologies as a mechanism to escape host defences, but also diverge into different ecomorphs related to the way they escape these defences. Lice that co-occur with other genera on a host exhibit greater morphological divergence, indicating a potential role of competition in evolutionary divergence.

Keywords: CT scanning; bird lice; co-adaptations; evolution; micro-morphology.

Figure 1.

Phylogenomic relationships between feather louse genera belonging to four ecomorph groups. Specimens and branches are coloured according to their ecomorph identification. The background colours represent the different bird host orders. The diamond shape on the nodes represents ecomorph transitions between sister taxa (red for lice parasitizing from the same host order, and yellow for lice parasitizing different host orders). AcidoproctusH, Acidoproctus hilli; AcidoproctusR, Acidoproctus rostratus; GoniodesO, Goniodes ortygis.

Figure 2.

Feather louse morphospace. Principal component analysis (PCA) results of generalized Procrustes analysis of 14 landmark data representing the head shape of 88 specimens belonging to four ecomorph groups (body, generalist, head and wing). PC1 (x) explains 53.5% of variability; PC2 (y) explains 10.49%. The coloured polygons represent the ecomorph group morphospace, with the mean PC1 and PC2 values for each ecomorph marked by an ×. The brighter red background colour polygon shows data including three Acidoproctus specimens (points 64–66), with the unusual head shape making their representation in the wing ecomorph group unclear. The dotted lines represent the space in which specimens (darker points) that do not co-occur with other ecomorphs on their hosts are found. The points outside those dotted lines represent lice that co-occur with other lice species on the same host, demonstrating that they reside in a more extreme morphospace, whereas all the lice that do not co-occur are found closer to the means of each ecomorph space.

Figure 3.

Phylo-morphospace analysis of louse ecomorphs. (a) A phylogenetic principal component analysis (phy-PCA) with centring and projections via ordinary least squares (OLS); (c) phy-PCA with centring and projections via generalized-least squares (GLS); (b) a phylogenetically aligned PCA (PACA) with OLS; (d) PACA with GLS.

Figure 4.

Mandibular muscularization of feather louse ecomorphs. (a) Proportional volume of the chewing muscles to the volume of the head (N = 77, or 79 with Acidoproctus). Asterisks indicate significant differences between group comparisons (***p < 0.001). The pink colour shows data including two Acidoproctus specimens, which have a strongly indented marginal carina between frontal projections, affecting the total volume of the head. (b) CT scan image of the head of four ecomorph groups with the mandibular muscles highlighted in pink.

Figure 5.

Proportional length of legs for each ecomorph group. (a) Illustrated louse morphology; (b) proportional length of legs (femur and tibia together) to metanotum width; (c) proportional length of leg parts (femur and tibia separately) to metanotum width. Asterisk shows significant differences between wing ecomorph and all other groups; hash shows significant differences between the wing and both head and body groups; the letter H shows a significant difference between wing and head ecomorphs.