Shifts in reproductive assurance strategies and inbreeding costs associated with habitat fragmentation in Central American mahogany

Abstract

The influence of habitat fragmentation on mating patterns and progeny fitness in trees is critical for understanding the long-term impact of contemporary landscape change on the sustainability of biodiversity. We examined the relationship between mating patterns, using microsatellites, and fitness of progeny, in a common garden trial, for the insect-pollinated big-leaf mahogany, Swietenia macrophylla King, sourced from forests and isolated trees in 16 populations across Central America. As expected, isolated trees had disrupted mating patterns and reduced fitness. However, for dry provenances, fitness was negatively related to correlated paternity, while for mesic provenances, fitness was correlated positively with outcrossing rate and negatively with correlated paternity. Poorer performance of mesic provenances is likely because of reduced effective pollen donor density due to poorer environmental suitability and greater disturbance history. Our results demonstrate a differential shift in reproductive assurance and inbreeding costs in mahogany, driven by exploitation history and contemporary landscape context.

Mating system and early viability resistance to habitat fragmentation in a bird-pollinated eucalypt

“…In fragmented tree populations, habitat loss and reduced stand density frequently disrupts pollination, which in turn alters mating patterns and gene flow dynamics (Ghazoul, 2005;Sork and Smouse, 2006). A common consequence of lower density is that altered pollination dynamics increases inbreeding (Lowe et al, 2005;Eckert et al, 2010;Breed et al, 2012) and/or reduces pollen diversity (Lowe et al, 2005;Breed et al, 2012). Nonetheless, this is not always the case (Bacles and Jump, 2011), and impacts can be highly contextdependent and affected by pollen vectors (Sork and Smouse, 2006;Eckert et al, 2010;Breed et al, 2012).…”

“…Indeed, as far as we are aware, there are currently only five published studies of open-pollinated Neotropical trees that have associated changes in mating patterns of individual trees caused by habitat disturbance with proxies of fitness (Rocha and Aguilar, 2001;Cascante et al, 2002;Fuchs et al, 2003;Quesada et al, 2004;Breed et al, 2012), and a single study conducted from Japan (Hirayama et al, 2007). As expected, selfing (4 of 6 studies), biparental inbreeding (2 of 3 studies) and correlated paternity (3 of 4 studies) tended to be negatively associated with fitness.…”

“…Individual-level statistical analyses of height used raw height (hereafter height), and implemented block and family as random effects (see below for more details on statistical analyses). Family-level statistical analyses of height used block-standardised height (hereafter height std ) methods, as described in Breed et al, (2012). To standardise the height for variation among blocks, the raw height of the i th seedling from the b th block (h ib ) was measured 10 months post-germination.…”

“…A common consequence of lower density is that altered pollination dynamics increases inbreeding (Lowe et al, 2005;Eckert et al, 2010;Breed et al, 2012) and/or reduces pollen diversity (Lowe et al, 2005;Breed et al, 2012). Nonetheless, this is not always the case (Bacles and Jump, 2011), and impacts can be highly contextdependent and affected by pollen vectors (Sork and Smouse, 2006;Eckert et al, 2010;Breed et al, 2012). To overcome this contextdependant effect, studies can investigate individuals within a single population that vary in their stand density (for example, Mimura et al, 2009;Llorens et al, 2012).…”

Constraints to and conservation implications for climate change adaptation in plants

“…Fragmentation may also hamper the flow of adaptive alleles from lower to higher latitudes or altitudes, restricting the adaptive potential of populations. Although estimates of long distance gene flow suggest that genes can move more quickly than is required to track climatic shifts (Kremer et al 2012), metaanalyses examining the genetic effects of habitat fragmentation have shown that fragmentation has a large and negative impact on population level genetic diversity and outcrossing rates (Lowe et al 2005a;Honnay and Jacquemyn 2007;Aguilar et al 2008;Eckert et al 2010;Breed et al 2012a;Vranckx et al 2012;Breed et al 2015). This seems to be the case for common species experiencing fragmentation as much as for rarer species, suggesting that vulnerability to genetic erosion and loss of genetic diversity is a common reality for plants in fragmented habitats (Honnay and Jacquemyn 2007).…”