Host defense reinforces host-parasite cospeciation

Abstract

Cospeciation occurs when interacting groups, such as hosts and parasites, speciate in tandem, generating congruent phylogenies. Cospeciation can be a neutral process in which parasites speciate merely because they are isolated on diverging host islands. Adaptive evolution may also play a role, but this has seldom been tested. We explored the adaptive basis of cospeciation by using a model system consisting of feather lice (Columbicola) and their pigeon and dove hosts (Columbiformes). We reconstructed phylogenies for both groups by using nuclear and mitochondrial DNA sequences. Both phylogenies were well resolved and well supported. Comparing these phylogenies revealed significant cospeciation and correlated evolution of host and parasite body size. The match in body size suggested that adaptive constraints limit the range of hosts lice can use. We tested this hypothesis by transferring lice among hosts of different sizes to simulate host switches. The results of these experiments showed that lice cannot establish viable populations on novel hosts that differ in size from the native host. To determine why size matters, we measured three components of louse fitness: attachment, feeding, and escape from host defense (preening). Lice could remain attached to, and feed on, hosts varying in size by an order of magnitude. However, they could not escape from preening on novel hosts that differed in size from the native host. Overall, our results suggest that host defense reinforces cospeciation in birds and feather lice by preventing lice from switching between hosts of different sizes.

Fig. 1.

Phylogenies of pigeons/doves and their feather lice in the genus Columbicola. Numbers after the names Columbicola passerinae, macrourae, and columbae indicate cryptic species of lice (17). Numbers beside branches are percent of 100-ML bootstrap replicates containing the node; values below 50% are not shown. Thin lines show host–parasite associations (17, 43). Fourteen of the 19 Columbicola species (74%) are host-specific. The remaining five species (bold) occur on two or more species of hosts. Circles with letters show cospeciation events inferred between the host and parasite trees by using reconciliation analysis (44). The eight cospeciation events are more than expected by chance (P = 0.029). Reconciliation analysis of trees derived from parsimony analyses of DNA sequences for doves and lice also inferred eight cospeciation events (P = 0.035). Asterisks show the five host species used in the experimental work.

Fig. 3.

Percent of lice remaining attached to grafts from feathers (drawn to scale) of four novel host species, compared to the native host (gray bars and feathers). The host species varied in size by more than an order of magnitude: C.G-d., Common Ground-dove (C. passerina), 30 g; M.D., Mourning Dove (Zenaida macroura), 119 g; W-t.D., White-tipped Dove (Leptotila verreauxi), 153 g; B-t.P., Band-tailed Pigeon (Patagioenas fasciata), 343 g; and the control, R.P., Rock Pigeon (C. livia), 355 g (29). The number of lice remaining attached did not differ significantly on Rock Pigeons allowed to fly a distance of 50–100 m (a) or on feathers taped to a high-speed fan for 20 min (b).

Fig. 2.

Relationship of parasite body size to host body size across the associations shown in Fig. 1. For the five nonspecific lice (Fig. 1), the mean body mass of their different host species was used. [Reproduced with permission from ref. (Copyright 2003, University of Chicago Press).]

Fig. 4.

(a) Number of C. columbae (mean ± SE) after 1 month in tubes containing feathers (drawn to scale) from one of four novel host species (black squares) or the native host (gray squares). Dotted line shows the number of lice placed in each tube at the start of the trial. (b) Mean (±SE) feather mass consumed per louse per tube during the trials. Host abbreviations are as in Fig. 3.

Fig. 5.

Population sizes (mean ± SE) of Rock Pigeon lice (C. columbae) transferred to novel host species, relative to the native host (gray bird). Host abbreviations are as in Fig. 3. Note log scale on y axis. Open squares are bitted birds that could not preen; closed squares are birds with normal preening ability (n = 6 birds per square, except W-t.D., n = 5 per square). Dotted line shows the number of lice transferred to each bird at the start of the experiment, which lasted 2 months. *, P < 0.01; †, P ≤ 0.05; for Dunnett's post hoc comparisons of the number of lice on each novel host species, relative to the number on Rock Pigeons (within preening treatments).