Speciation on oceanic islands: rapid adaptive divergence vs. cryptic speciation in a Guadalupe Island songbird (Aves: Junco)

Abstract

The evolutionary divergence of island populations, and in particular the tempo and relative importance of neutral and selective factors, is of central interest to the study of speciation. The rate of phenotypic evolution upon island colonization can vary greatly among taxa, and cases of convergent evolution can further confound the inference of correct evolutionary histories. Given the potential lability of phenotypic characters, molecular dating of insular lineages analyzed in a phylogenetic framework provides a critical tool to test hypotheses of phenotypic divergence since colonization. The Guadalupe junco is the only insular form of the polymorphic dark-eyed junco (Junco hyemalis), and shares eye and plumage color with continental morphs, yet presents an enlarged bill and reduced body size. Here we use variation in mtDNA sequence, morphological traits and song variables to test whether the Guadalupe junco evolved rapidly following a recent colonization by a mainland form of the dark-eyed junco, or instead represents a well-differentiated "cryptic" lineage adapted to the insular environment through long-term isolation, with plumage coloration a result of evolutionary convergence. We found high mtDNA divergence of the island lineage with respect to both continental J. hyemalis and J. phaeonotus, representing a history of isolation of about 600,000 years. The island lineage was also significantly differentiated in morphological and male song variables. Moreover, and contrary to predictions regarding diversity loss on small oceanic islands, we document relatively high levels of both haplotypic and song-unit diversity on Guadalupe Island despite long-term isolation in a very small geographic area. In contrast to prevailing taxonomy, the Guadalupe junco is an old, well-differentiated evolutionary lineage, whose similarity to mainland juncos in plumage and eye color is due to evolutionary convergence. Our findings confirm the role of remote islands in driving divergence and speciation, but also their potential role as repositories of ancestral diversity.

Figure 1. Geographic distributions and sampling localities of the different junco populations.

A. Distribution map of the genus Junco showing schematics of main plumage morphs. Lineage abbreviations, clockwise from south, are the following: VOJU (volcano junco J. vulcani), YEJU (yellow-eyed junco J. phaeonotus), and the following dark-eyed junco (J. hyemalis) morphs: GUJU (Guadalupe junco J. h. insularis), GHJU (gray-headed junco J. h. caniceps), ORJU (Oregon junco J. h. oreganus), SCJU (slate-colored junco J. h. hyemalis) and PSJU (pink-sided junco J. h. mearnsi). Sampling localities for each morph are marked with colored dots. B. Relative position of Guadalupe island with respect to the California shoreline. Juncos on the island are restricted to patches of cypress forest on the northern central plateau (dark green) and the few pine areas along the northern ridge (brown). Main junco distribution ranges are delimited by light green areas.

Figure 2. Photographs of individual males of the five junco morphs included in the study.

A. Oregon junco (J. h. oreganus), B. gray-headed junco (J. h. caniceps), C. pink-sided junco (J. h. mearnsi) D. yellow-eyed junco (J. phaeonotus) and E. Guadalupe junco (J. h. insularis). Note the plumage similarity between C and E.

Figure 3. Mitochondrial DNA haplotype networks of Guadalupe, continental North America and volcano juncos (VOJU).

Shown are median-joining networks for the concatenated CR and COI sequences (A), COI (B) and CR (C). Haplotypes are represented by circles, their size proportional to their frequency in the population. Color patterns are as follows: orange – Junco phaeonotus, blue tones – continental Junco hyemalis (dark: ORJU, light: PSJU, purple: GHJU), green – Junco h. insularis. Each branch represents a single nucleotide change, with additional mutations indicated by bars along branches. Numbers in squares indicate nucleotide changes separating the volcano junco.

Figure 4. Discriminant function analysis of morphological variables from the different junco lineages.

J. h. insularis (green squares), J. h. oreganus (blue squares), J. h. mearnsi (blue circles), J. h. caniceps (purple triangles) and J. phaeonotus (yellow circles). Empty circles represent group centroids. Correlation values between discriminant functions and transformed morphological variables are shown in table 4.

Figure 5. Differences in morphological trait means among junco lineages.

Bars correspond to 95% confidence intervals. Abbreviations correspond to Guadalupe junco (GUJU), continental dark-eyed juncos (DEJU) and yellow-eyed junco (YEJU). Units of measurement for weight are grams, and wing, tail, tarsus and bill variables are in mm.

Figure 6. Song spectrograms for representative song types from the three junco lineages.

A. J. h. oreganus, B. J. phaeonotus and C. J. h. insularis. Amplitude (y-axis) is given in KHz, and time (x-axis) is in seconds.

Figure 7. Discriminant function analysis of song variables for the three junco lineages.

J. h. insularis (green squares), J. h. oreganus (blue triangles) and J. phaeonotus (orange circles). Empty circles represent group centroids. See Table 5 for correlation values between discriminant functions and song variables