Long-term ‘islands’ in the landscape: low gene flow, effective population size and genetic divergence in the shrubHakea oldfieldii(Proteaceae)

Abstract

The genetic structure of disjunct populations is determined by founding genetic properties, demographic processes, gene flow, drift and local selection. We aim to identify the genetic consequences of natural population disjunction at regional and local scales in Hakea oldfieldii using nuclear and plastid markers to investigate long‐term effective population sizes and gene flow, and patterns of diversity and divergence, among populations. Regional divergence was significant as shown by a consistent pattern in principal coordinates, neighbor‐joining and Bayesian analyses, but divergence at the local level was also significant with localized distribution of plastid haplotypes and populations clustering separately in Bayesian analyses. Historical, recent and first‐generation gene flow was low, suggesting that recent habitat fragmentation has not reduced gene migration significantly. Genetic bottlenecks were detected in three populations. Long‐term effective population size was significantly correlated with the number of alleles/locus and observed heterozygosity, but not with census population size, suggesting that the loss of diversity is associated with long‐term changes rather than recent fragmentation. Inbreeding coefficients were significant in only three populations, suggesting that the loss of diversity is linked to drift and bottlenecks associated with demographic processes (local extinction by fires) rather than inbreeding. Historical disjunction as a result of specific ecological requirements, contraction of habitats following drying during the Pleistocene, low gene flow and changes in population size are likely to have been important forces driving divergence through isolation by distance and drift. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 179, 319–334.

Limiting inbreeding in disjunct and isolated populations of a woody shrub

“…Little is known of the mating system of H. oldfieldii. In the study of Sampson et al (2015), inbreeding coefficients were positive (F = 0.036-0.198) but did not indicate that inbreeding was an important component of the breeding system in 10 of 14 populations, and were not positively correlated with long-term effective population size.…”

“…But these reviews included relatively few studies of species with naturally disjunct population distributions. Several studies of plant species with disjunct distributions have found that genetic diversity is unrelated to census population sizes (Hoebee and Young 2001;Llorens et al 2004;Leimu and Mutikainen 2005;Mathiasen et al 2007;Sampson et al 2015). Indeed, it has been suggested (Holmes et al 2009;Hopper 2009) that naturally disjunct species may have ecological and genetic features that counter the negative effects of small size and isolation.…”

“…Populations are prone to fluctuations in size and extirpation because, although the species can be long-lived (>50 years), plants are killed by fire that occurs frequently in the shrublands of southwestern Australia. A recent study (Sampson et al 2015) suggested that low gene flow (N m < 1.0), below the level required to reduce the harmful effects of local inbreeding (N m > 1.0; Lowe and Allendorf 2010), genetic drift, and a demographic history of fluctuating population sizes including genetic bottlenecks have been the major determinants of the level and distribution of diversity in H. oldfieldii. Both long-term historical and contemporary migration were very low (contemporary migration rate, m = 0.001, long-term m = 0.003) among populations that show moderate levels of diversity and significant nuclear (microsatellite) and plastid divergence.…”

Anthropogenic fragmentation may not alter pre‐existing patterns of genetic diversity and differentiation in perennial shrubs

“…Other studies have similarly emphasized the persistence of prefragmentation patterns (Aguilar et al, 2008;Honnay, Adriaens, Coart, Jacquemyn, & Rold an-Ruiz, 2007;Menges, Dolan, Pickert, Yahr, & Gordon, 2010;Sampson et al, 2015). For example, the influence of historical landscape connectivity on gene flow accounted for the genetic similarity of currently fragmented populations of Globularia bisnagarica in Belgium , while long-term low effective population sizes arising from natural population fluctuations, rather than recent habitat fragmentation, explained low diversity within some populations of Hakea oldfieldii (also Proteaceae from an OCBIL; Sampson et al, 2015). These findings highlight the substantial role that fundamental aspects of biology, ecology and evolution can have in determining population genetic characteristics (Cole, 2003;Duminil et al, 2009;Hamrick & Godt, 1996) and demonstrate that these must be fully considered when interpreting the results of investigations into the effects of relatively recent habitat fragmentation.…”

“…The level of fine-scale structure was higher for G. longifolia (b AE SE = À0.063 AE 0.008; S p = 0.066) than G. caleyi (b AE SE = À0.036 AE 0.008; S p = 0.039). Other studies have similarly emphasized the persistence of prefragmentation patterns (Aguilar et al, 2008;Honnay, Adriaens, Coart, Jacquemyn, & Rold an-Ruiz, 2007;Menges, Dolan, Pickert, Yahr, & Gordon, 2010;Sampson et al, 2015). For example, the influence of historical landscape connectivity on gene flow accounted for the genetic similarity of currently fragmented populations of Globularia bisnagarica in Belgium , while long-term low effective population sizes arising from natural population fluctuations, rather than recent habitat fragmentation, explained low diversity within some populations of Hakea oldfieldii (also Proteaceae from an OCBIL; Sampson et al, 2015).…”