Rapid morphological divergence following a human-mediated introduction: the role of drift and directional selection

Abstract

Theory predicts that when populations are established by few individuals, random founder effects can facilitate rapid phenotypic divergence even in the absence of selective processes. However, empirical evidence from historically documented colonisations suggest that, in most cases, drift alone is not sufficient to explain the rate of morphological divergence. Here, using the human-mediated introduction of the silvereye (Zosterops lateralis) to French Polynesia, which represents a potentially extreme example of population founding, we reassess the potential for morphological shifts to arise via drift alone. Despite only 80 years of separation from their New Zealand ancestors, French Polynesian silvereyes displayed significant changes in body and bill size and shape, most of which could be accounted for by drift, without the need to invoke selection. However, signatures of selection at genes previously identified as candidates for bill size and body shape differences in a range of bird species, also suggests a role for selective processes in driving morphological shifts within this population. Twenty-four SNPs in our RAD-Seq dataset were also found to be strongly associated with phenotypic variation. Hence, even under population founding extremes, when it is difficult to reject drift as the sole mechanism based on rate tests of phenotypic shifts, the additional role of divergent natural selection in novel environments can be revealed at the level of the genome.

The Genomic Landscape of Divergence Across the Speciation Continuum in Island-Colonising Silvereyes (Zosterops lateralis)

“…Given that French Polynesia is located well beyond the natural distribution limit for this species and that the Mainland (Australia) vs. Heron Island: The Heron Island silvereye population was established from the mainland silvereye subspecies (Z. l. cornwalli) between 3,000-4,000 years ago. This divergence timeframe is supported by geological records which suggest that Heron Island has been vegetated (and therefore habitable) for a maximum of 4,000 years (Degnan and Moritz 1992;Hopley 1982 (Clegg et al 2002a;Sendell-Price et al 2020), Z. l. chlorocephalus from Heron Island is approximately 40% larger than its mainland ancestor Z. l. cornwalli (Clegg et al 2008), Z. l. melanops from Lifou is larger in many traits than its Grand Terre ancestor, Z. l. griseonotus (Black, R., unpublished results) and Z. l. tephropleurus from Lord Howe Island is substantially larger than its mainland ancestor (Clegg et al 2002a; Clegg and Phillimore 2010).…”

“…Given that the silvereye population in French Polynesia was the product of a human introduction and therefore likely had lower effective founder size than natural colonisations involving large expanding populations of silvereyes ( Sendell-Price et al 2020 ), we cannot rule out that the more wide-spread genomic divergence observed for the South Island vs. French Polynesia population comparison (when compared to other early stage comparison: South Island vs. Chatham Island) is the product of a potential severe population bottleneck during introduction. The potential for population founding to accelerate the accumulation of genomic differences has been highlighted previously ( Ravinet et al 2017 ), and in the silvereye system could be addressed through genomic comparisons of a number of other populations with varying intensities of population bottlenecks ( Estoup and Clegg 2003 ).…”

“…The French Polynesia silvereye population is the product of a documented human-mediated introduction of South Island silvereyes ( Z. l. lateralis ) to Tahiti in 1937 ( Monnet et al 1993 ; Thibault and Cibois 2017 ). Given that French Polynesia is located well beyond the natural distribution limit for this species and that the French Polynesian population is thought to be the product of a single and recent introduction event ( Sendell-Price et al 2020 ), this comparison is characterized as Early Stage – No Gene Flow.…”

“…For each of the population comparisons used in this study the diverging populations show body size differentiation. Z. l. lateralis from Chatham Island and French Polynesia are larger than those from their South Island source ( Clegg et al 2002a ; Sendell-Price et al 2020 ), Z. l. chlorocephalus from Heron Island is approximately 40% larger than its mainland ancestor Z. l. cornwalli ( Clegg et al 2008 ), Z. l. melanops from Lifou is larger in many traits than its Grand Terre ancestor, Z. l. griseonotus (Black, R., unpublished results) and Z. l. tephropleurus from Lord Howe Island is substantially larger than its mainland ancestor ( Clegg et al 2002a ; Clegg and Phillimore 2010).…”

“…Output from Satsuma Synteny was then used to assign scaffolds to chromosomes and determine order, location, and orientation using custom R scripts from Van Doren et al (2017) . Custom scripts from Sendell-Price et al (2020) were then used to reorder the GATK outputted VCF file accordingly and remove SNPs where chromosomal positions could not be determined. Because synteny is high in birds ( Ellegren 2010 ), 96.8% of the Zosterops scaffolds were assigned to assembled chromosomes and arranged in the presumed correct order and orientation.…”