Did postglacial sea-level changes initiate the evolutionary divergence of a Tasmanian endemic raptor from its mainland relative?

Abstract

Populations on continental islands are often distinguishable from mainland conspecifics with respect to body size, appearance, behaviour or life history, and this is often congruent with genetic patterns. It is commonly assumed that such differences developed following the complete isolation of populations by sea-level rise following the Last Glacial Maximum (LGM). However, population divergence may predate the LGM, or marine dispersal and colonization of islands may have occurred more recently; in both cases, populations may have also diverged despite ongoing gene flow. Here, we test these alternative hypotheses for the divergence between wedge-tailed eagles from mainland Australia (Aquila audax audax) and the threatened Tasmanian subspecies (Aquila audax fleayi), based on variation at 20 microsatellite loci and mtDNA. Coalescent analyses indicate that population divergence appreciably postdates the severance of terrestrial habitat continuity and occurred without any subsequent gene flow. We infer a recent colonization of Tasmania by marine dispersal and cannot discount founder effects as the cause of differences in body size and life history. We call into question the general assumption of post-LGM marine transgression as the initiator of divergence of terrestrial lineages on continental islands and adjacent mainland, and highlight the range of alternative scenarios that should be considered.

Keywords: Last Glacial Maximum; inbreeding depression; marine dispersal; sea level; subspecies; vicariance.

Figure 1.

Potential divergence scenarios of lineages from a continental island and adjacent mainland. Black bars represent lineages occupying the mainland, while crosshatched bars are lineages occupying islands (in these examples, the mainland is assumed to be the ancestral distribution, but the opposite is also possible). Arrows represent gene flow between lineages (here illustrated as bidirectional, but may also be unidirectional). Grey shading indicates periods of glaciation. (a,b) Vicariant divergence mediated by the most recent marine transgression. (c,d) An earlier divergence, with lineages maintaining their distinction through subsequent low sea stands, either with or without gene flow between lineages during glacial or interglacial periods. (e,f) Divergence initiated by marine dispersal, either with or without subsequent gene flow.

Figure 2.

Distribution of A. audax samples employed for genetic analysis from (a) Tasmania (A. a. fleayi, n = 175) and (b) mainland Australia (A. a. audax, n = 49). Note that two mainland and 60 Tasmanian individuals are not illustrated owing to the absence of fine-scale collection locality information.

Figure 3.

Minimum spanning network among mitochondrial haplotypes in A. audax. Circles represent haplotypes, with areas proportional to numbers of observations (smallest circles represent 1 individual, largest circle represents 35, others defined by the scale). Black shading represents mainland individuals (30 observations, slice of central haplotype corresponds to five individuals), white shading represents Tasmanian individuals. Lines linking haplotypes represent single mutation steps.

Figure 4.

Estimated population structure from STRUCTURE analysis. Each individual is represented by a vertical bar proportional to its estimated membership to the mainland (black) or Tasmanian (white) population, with the actual source of the individual demarcated along the top of the figure.

Figure 5.

Posterior distributions from analysis under the ‘Isolation with Migration’ model, indicated with black curves. Gene flow prior distributions (grey curves) are illustrated to demonstrate that the posterior distributions differ from them. (a) θ Tasmania, (b) θ mainland, (c) divergence time, (d) gene flow, mainland to Tasmania, going backwards in time, (e) gene flow, Tasmania to mainland, going backwards in time. Ne is effective population size, µ is mutation rate per generation, t is time since population splitting, and m is migration rate (gene flow).