Convergent evolution in dippers (Aves, Cinclidae): The only wing-propelled diving songbirds

Abstract

Of the more than 6,000 members of the most speciose avian clade, Passeriformes (perching birds), only the five species of dippers (Cinclidae, Cinclus) use their wings to swim underwater. Among nonpasserine wing-propelled divers (alcids, diving petrels, penguins, and plotopterids), convergent evolution of morphological characteristics related to this highly derived method of locomotion have been well-documented, suggesting that the demands of this behavior exert strong selective pressure. However, despite their unique anatomical attributes, dippers have been the focus of comparatively few studies and potential convergence between dippers and nonpasseriform wing-propelled divers has not been previously examined. In this study, a suite of characteristics that are shared among many wing-propelled diving birds were identified and the distribution of those characteristics across representatives of all clades of extant and extinct wing-propelled divers were evaluated to assess convergence. Putatively convergent characteristics were drawn from a relatively wide range of sources including osteology, myology, endocranial anatomy, integument, and ethology. Comparisons reveal that whereas nonpasseriform wing-propelled divers do in fact share some anatomical characteristics putatively associated with the biomechanics of underwater "flight", dippers have evolved this highly derived method of locomotion without converging on the majority of concomitant changes observed in other taxa. Changes in the flight musculature and feathers, reduction of the keratin bounded external nares and an increase in subcutaneous fat are shared with other wing-propelled diving birds, but endocranial anatomy shows no significant shifts and osteological modifications are limited. Muscular and integumentary novelties may precede skeletal and neuroendocranial morphology in the acquisition of this novel locomotory mode, with implications for understanding potential biases in the fossil record of other such transitions. Thus, dippers represent an example of a highly derived and complex behavioral convergence that is not fully associated with the anatomical changes observed in other wing-propelled divers, perhaps owing to the relative recency of their divergence from nondiving passeriforms.

Keywords: Cinclus; Pan-Alcidae; Pan-Sphenisciformes; Passeriformes; Pelecanoididae; Plotopteridae; endocast; ethology; integument; myology; osteology.

FIGURE 1

Map depicting the geographic ranges of wing‐propelled diving clades. Ranges for extant species correspond to those summarized in del Hoyo et al. (1992, 1996, 2005). The geographic range of Pan‐Alcidae extended further to the south in the Western Atlantic Ocean as recently as the Pleistocene (Smith & Clarke, 2015). Fossil localities for Plotopteridae are those summarized by Mayr et al. (2015)

FIGURE 2

An American Dipper Cinclus mexicanus (photo courtesy of D. Field). Note the robust and strongly curved unguals, short tail, and narial slit

FIGURE 3

Systematic position of wing‐propelled diving birds (bolded) and their near outgroups in Aves. The tree is simplified from Ksepka et al. (2020) with the position of Cinclidae modified based on Oliveros et al. (2019) and the position of Plotopteridae based on Mayr et al. (2021)

FIGURE 4

Beaks of wing‐propelled divers in lateral view showing the slit‐like external nares (n): (a) Cinclus mexicanus (Cinclidae, American Dipper; USNM 530549) and (b) Fratercula cirrhata (Alcidae, Tufted Puffin; USNM 589729)

FIGURE 5

Brain endocasts of a, d, g, j, Catharus guttatus (Turdidae, Hermit Thrush, USNM 634096); b, e, h, k, Aplonis atrifusca (Sturnidae, Samoan Starling, USNM 498061); and c, f, i, l, Cinclus mexicanus (Cinclidae, American Dipper, USNM 630605) in left lateral view (a–c), ventral view (d–f), dorsal view (g–i), and caudal views (j–l), all based on surface renders of μCT scan data. Anatomical abbreviations: Cbl, cerebellum; cer, cerebral hemisphere; lab, endosseous labyrinth; opt, optic lobe; W, wulst. Scale bar = 1 cm

FIGURE 6

Medial views of the right side of sagittally sectioned skulls (based on volume renders of μCT scan data) of a, Aplonis atrifusca (Sturnidae, Samoan Starling, USNM 498061); b, Catharus guttatus (Turdidae, Hermit Thrush, USNM 634096); and c, Cinclus mexicanus (Cinclidae, American Dipper, USNM 630605); d, Pelecanoides urinatrix (YPM 120642) showing the minor differences in the extent of craniofacial pneumaticity. Anatomical abbreviations: Br, basicranial recesses; dr, dorsal recesses; er, ethmoid recesses; tc, trabecular cells. Scale bars = 1 cm

FIGURE 7

Sterna of wing‐propelled divers (and a nonwing‐propelled diving gull for comparison) in ventral view: a, Cinclus pallasii (Cinclidae, Brown Dipper; USNM 319050); b, Larus marinus (Laridae, Black‐backed Gull; NCSM 10245); c, Aethia pusilla (Alcidae, Least Auklet; NCSM 17734); d, Cerorhinca monocerata (Alcidae, Rhinoceros Puffin; USNM 557614). All scale bars = 1 cm

FIGURE 8

Humeral cross‐sections showing the relative cortical bone thickness and dorsoventral compression of the mid‐shaft region: a, Cinclus mexicanus (Cinclidae, American Dipper; FMNH 288367); b, Catharus minimus (Turdidae, Gray‐cheeked Thrush; FLMNH 52130); c, Pelecanoides urinatrix (Pelecanoididae, Common Diving Petrel; YPM 120642); d, Alca torda (Alcidae, Razorbill; NCSM 22058); e, Aptenodytes forsteri (Spheniscidae, Emperor Penguin; AMNH 3728). Images not to scale for comparison

FIGURE 9

Humeri of wing‐propelled divers in ventral view: a, Cinclus cinclus (Cinclidae, White‐throated Dipper; USNM 499067); b, Pinguinus impennis (Alcidae, Great Auk; USNM 623465); c, Aptenodytes forsteri (Spheniscidae, Emperor Penguin; AMNH 8110). Anatomical abbreviations: dc, deltopectoral crest; dsp, dorsal supracondylar process; scs, supracoracoideus scar; ts, tricipital sulcus. Scale bars = 1 cm

FIGURE 10

Wing elements of a, Mancalla sp. (Alcidae, Lucas Auk; composite LACM 154560; modified from Smith (, fig. 16); not to scale; oblique dorsal view) and b, Cinclus mexicanus (Cinclidae, American Dipper; rendered from CT scan of FMNH 288367; oblique ventral view). Note that in Mancalla, the ulna is shorter than both the humerus and the carpometacarpus, a condition otherwise known only in hummingbirds among all extant Aves (Smith, 2011b). In contrast, the ulnae of dippers are longer than both the humerus and carpometacarpus but are also relatively shorter than the ulnae of thrushes. Scale bar = 3.5 mm

FIGURE 11

Carpometacarpi of a, Cinclus pallasii (Cinclidae, Brown Dipper; USNM 292206; also including digit II, phalanx 1, and digit III, phalanx 1); b, Alca torda (Alcidae, Razorbill; NCSM 20058), and c, Spheniscus demersus (Spheniscidae, African Penguin; SAM, uncatalogued) in ventral view. Anatomical abbreviations: ep, extensor process; MCI, first metacarpal. Scale bars = 1 cm

FIGURE 12

Distal wing elements of a, Cinclus pallasii (Cinclidae, Brown Dipper; USNM 319050); and b, Aptenodytes forsteri (Spheniscidae, Emperor Penguin; AMNH 3767) depicting the range of relative size of free carpals among wing‐propelled divers (dorsal view). Anatomical abbreviations: r, radiale; u, ulnare. Scale bars = 1 cm

FIGURE 13

Lateral view of scapulae. a, Cinclus cinclus (Cinclidae, White‐throated Dipper; USNM 637549); b, Catharus guttatus (Turdidae, Hermit Thrush; BM; uncatalogued); c, Pinguinus impennis (Alcidae, Great Auk; USNM 623465; modified from Smith (, fig. A2.22); d, Eudyptes chrysolophus (Spheniscidae, Macaroni Penguin; AMNH 5974; modified from Ksepka and Clarke (, fig. 24; not to scale). Anatomical abbreviations: acr, acomion; gf, glenoid facet; sb, scapular blade. Scale bars for Cinclus and Pinguinus = 25 mm. Scale bar for Catharus = 1 cm

FIGURE 14

Pygostyle and last free caudal vertebra in left lateral view: a, Cinclus cinclus (Cinclidae, White‐throated Dipper; USNM 637551); b, Alca torda (Alcidae, Razorbill; NCSM 20058). Scale bars = 1 cm

FIGURE 15

Cranial integument, narial morphology, and myological comparison: a, Cinclus mexicanus (Cinclidae, American Dipper); b, Catharus ustulatus (Turdidae, Swainson's Thrush). Note that in Cinclus the nares (n) are elongate slits; the sternum (s) is relatively elongate as compared to Catharus, and m. pectoralis major (p; on right of sternal keel in middle row) and m. supracoracoideus (s; on left of sternal keel in middle row) are relatively larger. Top row in right lateral view; middle row in ventral view; bottom row in left lateral view

FIGURE 16

Phylomorphospace showing the principal component axes 2 and 3 for Catharus and Cinclus. The two axes are those that characterize the major differences in length of elements and features between the two groups (the first axis is largely size). The loadings for each trait are shown on the top (for PC2) and at right (for PC3). The relationship between the supracondylar process and deltopectoral crest characterize PC3 which shows the greatest difference between the dippers and thrushes. Abbreviations: Deltop., deltopectoral crest; MCI, metacarpal one; Supracond., dorsal supracondylar process length; Supracora., supracoracoideus scar length; Tarso, tarsometatarsus; Tibio, tibiotarsus

FIGURE 17

Correlogram showing the pairwise correlation between skeletal elements of Catharus and Cinclus. A perfect correlation (r = 1) is represented as a line, while no correlation (r = 0) is represented as a perfect circle. Ovals indicate a correlation between 0 and 1, with a more circular shape indicating lower correlation. The sign of the correlation is indicated by both the orientation of the oval and by its color (red color and pointing towards the left upper corner indicates a negative correlation, and blue indicates a positive correlation). These phylogenetically corrected correlations were determined between elements within a genus according to the phylogenies from Jetz et al. (2012). a, Correlations in the genus Catharus showing some negative relationships between certain wing and leg traits (red). b, Correlations in the genus Cinclus showing that in dippers all elements scale positively with one another, although leg and wing traits have weaker correlations

FIGURE 18

Phylogenetic hierarchical regressions showing the best estimate of each genus‐specific regression of body mass against each osteological measurement. Standard Bayesian 50% confidence intervals are shown. Positive values equate to larger relative size. The ulna:humerus ratio and tarsometatarsus:tibiotarsus ratio show the greatest allometric difference between genera, although the divergence is not large enough to be statistically clear at the p < .05 level. Bayesian R ² values for the regressions are 0.91 ± 0.01 for keel length, 0.46 ± 0.08 for the deltopectoral crest, 0.40 ± 0.08 for supracondylar length, 0.84 ± 0.03 for pygostyle length, 0.82 ± 0.03 for ulna:humerus ratio, and 0.83 ± 0.03 for tarsometatarsus:Tibiotarsus ratio

FIGURE 19

Left endosseous labyrinths of the inner ear of a, d, g, Catharus guttatus (Turdidae, Hermit Thrush, USNM 634096); b, e, h, Aplonis atrifusca (Sturnidae, Samoan Starling, USNM 498061); and c, f, i, Cinclus mexicanus (Cinclidae, American Dipper, USNM 630605) in left lateral view (a–c), dorsal view (d–f), and caudal view (g–i), all based on surface renders of μCT scan data. Anatomical abbreviations: c, cochlear duct; cc, crus communis; csc, caudal semicircular canal; csca, ampulla of the caudal semicircular canal; fc, fenestra cochleae; fv, fenestra vestibuli; lsc, lateral semicircular canal; lsca, ampulla of the lateral semicircular canal; rsc, rostral semicircular canal; rsca, ampulla of the rostral semicircular canal. Scale bar = 0.5 cm

FIGURE 20

Skulls of a, Catharus guttatus (Turdidae, Hermit Thrush, USNM 634096); b, Aplonis atrifusca (Sturnidae, Samoan Starling, USNM 498061); and c, Cinclus mexicanus (Cinclidae, American Dipper, USNM 630605) in left lateral view (based on surface renders of μCT scan data) with the brain endocast and endosseous labyrinth superimposed in position. The lateral semicircular canals are oriented horizontally showing the natural alert posture of the head (Witmer et al., 2008) and the rotation of the brain to accommodate the large eyeball within the orbit. Scale bar = 1 cm

FIGURE 21

Comparison of wing shape of selected WPD birds in dorsal view: a, Catharus guttatus (Turdidae, Hermit Thrush; PSM 11204); b, Cinclus mexicanus (Cinclidae, American Dipper; USNM 640895); c, Aethia pusilla (Alcidae, Least Auklet; UWBM 48412); d, Pelecanoides urinatrix (Pelecanoididae, Common Diving Petrel; PSM 17233). Scale bars = 1 cm

FIGURE 22

Underside of preserved specimen of Cinclus leucocephalus (Cinclidae, White‐capped Dipper; USNM 387744) showing the thickened foot pads, large and strongly curved unguals, and short rectrices characteristic of dippers. Scale bar = 1 cm

FIGURE 23

Comparison of clade age and quantity of convergent characters associated with wing‐propelled diving. The range depicted for Plotopteridae includes the uncertainty that exists because of the current state of anatomical knowledge based on the clade's incomplete fossil records. Background image of wing elements (from left to right; Spheniscus, Mancalla, Pinguinus, Alca, Larus) modified from Storer (1960)