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Contemporary pollen-mediated gene immigration reflects the historical isolation of a rare, animal-pollinated shrub in a fragmented landscape.

ABSTRACT: Fragmentation is generally considered to have negative impacts on widespread outbreeders but impacts on gene flow and diversity in patchy, naturally rare, self-compatible plant species remain unclear. We investigated diversity, gene flow and contemporary pollen-mediated gene immigration in the rare, narrowly distributed endemic shrub Calothamnus quadrifidus ssp. teretifolius. This taxon occurs in an internationally recognized biodiversity hotspot subjected to recent human-induced fragmentation and the condition of the remnants ranges from intact to highly degraded. Using microsatellites, we found that inbreeding, historically low gene flow and significant population differentiation have characterized the genetic system of C. quadrifidus ssp. teretifolius. Inbreeding arises from self-pollination, a small amount of biparental inbreeding and significant correlation of outcross paternity but fecundity was high suggesting populations might have purged their lethals. Paternity analyses show that pollinators can move pollen over degraded and intact habitat but populations in both intact and degraded remnants had few pollen parents per seed parent and low pollen immigration. Genetic diversity did not differ significantly between intact and degraded remnants but there were signs of genetic bottlenecks and reduced diversity in some degraded remnants. Overall, our study suggests human-induced fragmentation has not significantly changed the mating system, or pollen immigration to, remnant populations and therefore genetic connectivity need not be the highest conservation priority. Rather, for rare species adapted to higher levels of inbreeding, conservation efforts may be best directed to managing intact habitats and ecosystem processes.

SUBMITTER: Sampson JF

PROVIDER: S-EPMC3907103 | biostudies-literature | 2014 Feb

REPOSITORIES: biostudies-literature

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Contemporary pollen-mediated gene immigration reflects the historical isolation of a rare, animal-pollinated shrub in a fragmented landscape.

Sampson J F JF Byrne M M Yates C J CJ Gibson N N Thavornkanlapachai R R Stankowski S S MacDonald B B Bennett I I

Heredity 20130925 2

Fragmentation is generally considered to have negative impacts on widespread outbreeders but impacts on gene flow and diversity in patchy, naturally rare, self-compatible plant species remain unclear. We investigated diversity, gene flow and contemporary pollen-mediated gene immigration in the rare, narrowly distributed endemic shrub Calothamnus quadrifidus ssp. teretifolius. This taxon occurs in an internationally recognized biodiversity hotspot subjected to recent human-induced fragmentation a ...[more]

PMID: 24065181

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Project description:IntroductionTheory predicts that habitat fragmentation, by reducing population size and increasing isolation among remnant populations, can alter their genetic diversity and structure. A cascade of effects is expected: genetic drift and inbreeding after a population bottleneck, changes in biotic interactions that may affect, as in the case of plants, pollen dynamics, mating system, reproductive success. The detection of the effects of contemporary habitat fragmentation on the genetic structure of populations are conditioned by the magnitude of change, given the few number of generations since the onset of fragmentation, especially for long-lived organisms. However, the present-day genetic structure of populations may bear the signature of past demography events. Here, we examine the effects of rainforest fragmentation on the genetic diversity, population structure, mating system (outcrossing rate), indirect gene flow and contemporary pollen dynamics in the understory herb Aphelandra aurantiaca. Also, we assessed its present-day genetic structure under different past demographic scenarios.MethodsTwelve populations of A. aurantiaca were sampled in large (4), medium (3), and small (5) forest fragments in the lowland tropical rainforest at Los Tuxtlas region. Variation at 11 microsatellite loci was assessed in 28-30 reproductive plants per population. In two medium- and two large-size fragments we estimated the density of reproductive plants, and the mating system by analyzing the progeny of different mother plants per population.ResultsDespite prevailing habitat fragmentation, populations of A. aurantiaca possess high genetic variation (He = 0.61), weak genetic structure (Rst = 0.037), and slight inbreeding in small fragments. Effective population sizes (Ne ) were large, but slightly lower in small fragments. Migrants derive mostly from large and medium size fragments. Gene dispersal is highly restricted but long distance gene dispersal events were detected. Aphelandra aurantiaca shows a mixed mating system (tm = 0.81) and the outcrossing rate have not been affected by habitat fragmentation. A strong pollen pool structure was detected due to few effective pollen donors (Nep ) and low distance pollen movement, pointing that most plants received pollen from close neighbors. Past demographic fluctuations may have affected the present population genetic structure as Bayesian coalescent analysis revealed the signature of past population expansion, possibly during warmer conditions after the last glacial maximum.DiscussionHabitat fragmentation has not increased genetic differentiation or reduced genetic diversity of A. aurantiaca despite dozens of generations since the onset of fragmentation in the region of Los Tuxtlas. Instead, past population expansion is compatible with the lack of observed genetic structure. The predicted negative effects of rainforest fragmentation on genetic diversity and population structure of A. aurantiaca seem to have been buffered owing to its large effective populations and long-distance dispersal events. In particular, its mixed-mating system, mostly of outcrossing, suggests high efficiency of pollinators promoting connectivity and reducing inbreeding. However, some results point that the effects of fragmentation are underway, as two small fragments showed higher membership probabilities to their population of origin, suggesting genetic isolation. Our findings underscore the importance of fragment size to maintain genetic connectivity across the landscape.

Project description:Background and aimsBecause distylous species have two hermaphroditic style-length floral morphs, they face two sex allocation problems: the equilibrium morph ratio and the optimal allocation to pollen and seed production in each floral morph. Gender specialization is expected among distylous species when floral morphs differ in reproductive output. However, spatio-temporal variability in female reproductive output between morphs needs to be investigated to fully understand patterns of sexual expression and gender specialization in distylous plants. Between-year variation in flower and fruit production of hummingbird-pollinated Palicourea padifolia (Rubiaceae) was examined, focusing on functional gender expression of long- and short-styled morphs and comparing their reproductive performance in five consecutive years (1998-2002).MethodsBetween-year variation in inflorescence, floral bud and fruit production was monitored and quantified. These traits were then used as parameters to determine functional gender differences between floral morphs through time.Key resultsInflorescence production varied among years but no significant differences were found between floral morphs. Long-styled plants initiated more floral buds per inflorescence every year than short-styled plants, suggesting higher allocation to pollinator attraction and, potentially, an increase in male fitness through pollen donation. Although fruit production was similar between morphs, their functional gender shifted across years.ConclusionsThe gender expression inconsistency across years is surprising because a number of floral characters and attributes that contribute to differently attracting and rewarding effective pollinators in P. padifolia suggest gender specialization. The evidence that morphs of distylous species might specialize in functional gender mostly comes from differences among populations in seed production and non-equilibrium morph ratios based on 1-year field population surveys. The results suggest that more sampling through time is needed to detect gender specialization among distylous species with a perennial habit.

Dataset Information

Contemporary pollen-mediated gene immigration reflects the historical isolation of a rare, animal-pollinated shrub in a fragmented landscape.

Publications

Contemporary pollen-mediated gene immigration reflects the historical isolation of a rare, animal-pollinated shrub in a fragmented landscape.

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