The relative importance of ecology and geographic isolation for speciation in anoles

Abstract

The biogeographic patterns in sexually reproducing animals in island archipelagos may be interpreted as reflecting the importance of allopatric speciation. However, as the forms are allopatric, their reproductive isolation is largely untestable. A historical perspective integrating geology and molecular phylogeny reveals specific cases where ancient precursor islands coalesce, which allows the application of population genetics to critically test genetic isolation. The Anolis populations on Martinique in the Lesser Antilles are one such case where species-level populations on ancient precursor islands (ca 6-8 Myr BP) have met relatively recently. The distribution of the mtDNA lineages is tightly linked to the precursor island, but the population genetic analysis of microsatellite variation in large samples shows no evidence of restricted genetic exchange between these forms in secondary contact. This tests, and rejects, the hypothesis of simple allopatric speciation in these forms. By contrast, Martinique has pronounced environmental zonation, to which anoles are known to adapt. The population genetic analysis shows restricted genetic exchange across the ecotone between xeric coastal habitat and montane rainforest. This does not indicate full ecological speciation in these forms, but it does suggest the relative importance of the role of ecology in speciation in general.

Figure 1

Lesser Antillean anoles. Distribution of the A. roquet series species in the south and the A. bimaculatus series in the north (A. wattsi group not shown).

Figure 2

Geological history of the components of Martinique. Two islands in (a) the older arc, Caravelle (east) and St Anne (south (s)), were subsequently joined by a further two islands at the origin of (b) the younger arc, northwest (nw) and southwest (sw). General uplifting of (c) the central area, (d) continued until the central area joined the peripheral precursor islands into (e) the present single island of Martinique.

Figure 3

Secondary contact zone and ecotone in northwest Martinique. The dashed line marks the geological boundary between the northwest and central regions where populations on these precursor islands may make secondary contact. The cross-hatched area represents the ecotone where the xeric coastal habitat (transect localities 1 and 2) is in transition to the montane rainforest (transect localities 4–7).

Figure 4

Phylogeny of Anolis roquet and associated species. This Bayesian tree shows the Barbadian species, A. extremus, is the sister lineage to central Martinique and is nested within the phylogenetically deeper divisions of A. roquet from the precursor islands, which are now in secondary contact. The terminal node numbers are the locality codes for Martinique in Thorpe & Stenson (2003) and Barbados in Thorpe et al. (2005b), which are followed by alphabetic codes for individual replicates, with E denoting A. extremus, and additional localities 93, S1 and S2 (located at UTM zone 20 coordinates E-720425/N-1630450, E-733300/N-1599225 and E-732157/N-1594585, respectively).

Figure 5

Transects showing (a) lineages, (b) selection regimes and (c) genotype structure. The transect localities (mapped in figure 3) are arranged in geographical order on the horizontal axis, with E representing the position of the ecotone (the switch between xeric coastal woodland and montane rainforest) and G the position of secondary contact between the northwest (localities 1–6) and central (7) geological regions. (a) The frequency (48 individuals per locality) of the northwest (black) and central (white) mtDNA lineages. (b) Mean first canonical variate (CVI) scores for adult males based on their quantitative traits (right-pointing filled triangles) and dewlap hue (left-pointing filled triangles), and the first principal coordinate score of environmental variables (open triangles). The CV scores are in units of 2 within group standard deviations. (c) The frequency of individuals (48 individuals per locality) assigned to the two Bayesian clusters, ‘xeric’ (white) and ‘montane rainforest’ (black), based on variation in nine unlinked microsatellites.

Figure 6

Dewlap hue. Examples of spectrophotometrically measured percentage reflectance across the near UV to red spectrum (in nm). (a) The anterior dewlap of a xeric woodland male is a dull greyish (including near UV) hue, which contrasts to the bright focal green hue of the montane rainforest male. (b) The posterior dewlap of the rainforest male is brighter, more focal yellow, than that of the xeric woodland male.