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New Forests DOI 10.1007/s11056-017-9604-6

Mating patterns of the gum arabic tree (Acacia senegal synonym Senegalia senegal) in two different habitats Stephen F. Omondi1,2 • David W. Odee1 • George O. Ongamo2 James I. Kanya2 • Damase P. Khasa3

Received: 30 October 2016 / Accepted: 27 July 2017 Ó Springer Science+Business Media B.V. 2017

Abstract Understanding the variation of mating patterns in disturbed habitats provide insight into the evolutionary potential of plant species and how they persist over time. However, this phenomenon is poorly understood in tropical dryland tree species. In the present study, we investigated how Acacia senegal reproduces in two different environmental contexts in Kenya. Open-pollinated progeny arrays of 10 maternal trees from each environmental context were genotyped using 12 nuclear microsatellite markers. Overall, A. senegal displayed a predominantly allogamous mating pattern. However, higher multilocus outcrossing rate (tm) was found in Lake Bogoria (tm = 1.00) than in Kampi ya Moto population (tm = 0.949). Higher biparental inbreeding (tm - ts = 0.116) and correlation of outcrossed paternity (rp = 0.329) was found in Kampi ya Moto than in Lake Bogoria population (tm - ts = 0.074, rp = 0.055), showing the occurrence of mating among relatives. Coefficient of coancestry (H = 0.208) showed that full-sibs constitute about 21% of the offspring in Kampi ya Moto population compared to about 14% (H = 0.136) in Lake Bogoria population. The results demonstrate that low adult tree density of A. senegal may be promoting seed production through consanguineous mating and suggest that manmade disturbance can affect mating patterns of the species. Despite these mating differences, trees from both populations can contribute as seed source for conservational plans, and to support effective genetic conservation and artificial regeneration programs of A. senegal. We suggest collection of seeds from at least 42 and 63 trees in Lake Bogoria and Kampi ya Moto populations, respectively, to retain a progeny array with a total effective population size of 150.

& Stephen F. Omondi stephenf.omondi@gmail.com 1

Kenya Forestry Research Institute, P.O. Box 20412-00200, Nairobi, Kenya

2

School of Biological Sciences, University of Nairobi, P.O. Box 30197-00100, Nairobi, Kenya

3

Centre for Forest Research and Institute for Systems and Integrative Biology (IBIS), Laval University, Sainte-Foy, QC G1V 0A6, Canada

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Keywords Anthropogenic disturbance  Biparental inbreeding  Genetic conservation  Mating system  Self-incompatibility  Acacia senegal

Introduction Mating system is an important determinant of genetic constitution of a tree population, and has a significant bearing on the subsequent generations, gene flow and natural selection (Millar et al. 2014; Kikuchi et al. 2015). In principle, mating system play major role in determining how genetic information is passed between generations and among populations, as well as the offspring fitness. However, tree species mating system is dynamic and can change with time and space (Eckert et al. 2010). Interestingly, heterogeneity of tree mating system has been found even among populations, within populations, and even between seasons (Lee et al. 2000). These variations may be influenced by several factors including human mediated disturbances, presence of self-incompatibility systems, pollinator activity and foraging behavior (Franceschinelli and Bawa 2000). Other factors may include phenological patterns, like flowering synchrony (Hall et al. 1996; Karasawa et al. 2007). Human disturbances are quite common in the tropical landscapes and they can bring negative effects on plant mating system and on the establishment of new plants (Eckert et al. 2010). For example, density and population size of adult trees may be reduced through selective harvesting, lowering the pollen diversity for fertilization (Feres et al. 2012; Duminil et al. 2016). Moreover, reduced gene flow between individual trees or populations and the reduction in reproductive population size may ultimately affect the genetic patterns, reducing offspring genetic diversity. This may largely be due to the few numbers of outcross mates, which limit the diversity of pollen sources and promote selffertilization in self-compatible species or mating among relatives (Lowe et al. 2005; Jacquemyn et al. 2012). This problem is quite common in tree species that require outcrossing mating patterns (Aguilar et al. 2008). In such cases, mating between closely related individuals (biparental inbreeding) are prevalent and may lead to an increase in the frequency of inbreeding incidences and maladaptation in subsequent generations (Feres et al. 2012). Knowledge of mating patterns and factors that are likely to affect it and the scale at which they operate are therefore essential in understanding the genetic structure of plant populations in anthropogenic-disturbed habitats that require restoration or conservation (Beardmore 1983; Alves et al. 2003; de-Lucas et al. 2008). Such information are useful in developing reliable genetic improvement and/or conservation programs (Frankham et al. 2011). Generally, changes in mating patterns will directly affect the quality of seed production including effective size of collected seeds, overall progeny genetic diversity, connectivity and structure of the populations (Millar et al. 2014). All these processes are important to the adaptive evolution of plant populations (Eckert et al. 2010). Breeding analyses have indicated possibilities of detecting shifting or variation in mating patterns at very small scales (Feres et al. 2012). Increased selfing and inbreeding depression have been revealed for selectively extracted or disturbed plant populations, when compared to undisturbed ones for some species (Tamaki et al. 2009 and the references therein). Other studies have shown that mating systems and seed production in many tropical trees species are affected by habitat disturbances (Lowe et al. 2005). This is generally due to their low densities and outcrossing mating patterns, pollinators and seed dispersers’ activity (Dick et al. 2003; Ward et al. 2005).

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Disruption of genetic connectivity occur when populations are fragmented and become small or genetically isolated (Fuchs et al. 2003). However, landscape heterogeneity and the land-use types play a significant role in the genetic connectivity (Lander et al. 2011). A disturbance that leads to habitat fragmentation may also affect the behavior of pollinators, restricting their movements. The effect of gene flow disruption may include increased selfing rate and mating among close relatives, leading to inbreeding in subsequent generations (Feres et al. 2012). Furthermore, reduction in the diversity of alleles within a population due to increased disturbances may lead to reduction in genetic variability and increased genetic differentiation (Young et al. 1996). For species conservation, genetic improvement and artificial plantation establishment purposes, in situ and ex situ preservation of genetic resources is essential. Some of these stands normally rely on openpollination to sustain genetic diversity (Ellstrand and Ellam 1993). Thus, investigating plant mating system in different environmental contexts, as well as investigating their relative importance and the scale at which they operate (population, stand or individual), is of great importance for conservation and evolution of a tree species (de-Lucas et al. 2008). Acacia senegal (L.) Willd (Syn. Senegalia Senegal), (Fabaceae) commonly known as gum arabic tree, is an important multipurpose tropical dryland tree species (Fagg and Allison 2004). The species is widely distributed in the arid and semi-arid environments, harboring great potentials for socio-economic and ecological benefits (Chikamai and Odera 2002; Wekesa et al. 2010; Diallo et al. 2015). Acacia senegal is generally outbreeding and is believed to have self-incompatibility mechanisms that may prevent self-fertilization, however, the species has been observed to set seeds in some occasions through selffertilization (Diallo et al. 1997, 2015; Tandon and Shivanna 2001). In Kenya, A. senegal is distributed and exploited in most of the dryland ecosystem, including Lake Baringo woodland (Omondi et al. 2010). Despite its wide distribution, ecological and economic values, several natural relict populations of A. senegal are threatened by habitat disturbances, evidenced by low densities and poor recruitments (Fagg and Allison 2004; Omondi et al. 2010, 2016a). These disturbances may affect the reproductive success of the species, which in the long run might threaten its adaptation. No study has been undertaken to determine the mating patterns of A. senegal populations in different environmental contexts. This information is of utmost importance to improve and develop conservation and tree improvement strategies for the species. The aim of the present study was to determine the mating patterns of A. senegal in two different habitats to support sustainable management and genetic conservation of the species. We thus specifically addressed the following questions: (1) Is there differences in mating system parameters between Lake Bogoria and Kampi ya Moto populations, (2) Does low density of adult trees promote consanguineous mating patterns in A. senegal and (3) Can seeds be collected from trees in the more disturbed area?

Materials and methods Study site and population disturbance levels Two natural populations of A. senegal, Kampi ya Moto (00째140 N and 36째350 E) and Lake Bogoria (00째210 N and 36째030 E), separated by about 75 km within Lake Baringo woodland ecosystem were studied. We classified the two populations as either lightly disturbed or heavily disturbed, based on population disturbance index (PDI) and density of adult trees.

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We determined the PDI by assessing and allocating values to different disturbance indicators within the study sites. The disturbance indicators used in determination of the index were; number of new settlements, presence of cultivated land, presence of grazing livestock, level of seedling browsing, number of cut tree stumps, number of charcoal kilns and number of fenced plots in the two populations. We calculated PDI for each population as the mean percentage of all the present indicators, following the procedure described by Omondi et al. (2016a). The above indicators used were those reported as the major factors affecting vegetation dynamics within Lake Baringo woodland ecosystem by the Baringo County Government (BCG 2014). Density of adult A. senegal trees in each population was determined by performing inventory in 15 plots measuring 20 9 20 m (400 m2) and the mean number of adult trees (diameter at breast height C5 cm) per hectare calculated for each population.

Sample collection Ten maternal trees were sampled randomly at a distance between 100 and 300 m apart in each population, giving a total of 20 adult trees. From each of the adult trees, we harvested healthy leaf tissues. The tissues were then dried in silica gel for transportation then latter kept at -4 °C in the laboratory until DNA isolation. In addition to the leaf samples, 40 open-pollinated seeds were collected per maternal tree and kept separately, giving a total of 400 seeds per population and 800 seeds for the two populations. The seeds were germinated per family in polythene tubes, and the germination rate was calculated. The seedlings grew for one month in the greenhouse condition. Leaf tissues were then collected from the seedlings for DNA isolation. Due to low germination in some families, 10–11 seedlings were genotyped per family. In this study, we referred to seedlings from a single maternal tree as progeny array or family.

DNA isolation and microsatellite analysis Total genomic DNA was isolated from 10 g of the leaf tissues collected from both maternal trees and the progenies using the protocol described by Hanaoka et al. (2013). Polymerase chain reaction (PCR) amplifications of 12 polymorphic nuclear microsatellite markers developed and optimized for A. senegal by Omondi et al. (2016a) were used to genotype both the seedlings and the maternal trees. The PCR program followed the procedure described by Omondi et al. (2016a). Capillary fragment electrophoresis of PCR products was scored against an internal standard (600 Liz size standards) on an Applied Biosystems, 3500 genetic analyser (Applied Biosystems, Califonia, USA). The genotype data was captured using GeneMapper 5.0 software (Applied Biosystems, Califonia, USA).

Mating system and data analyses We tested for the presence of null alleles using Micro-checker version 2.2.3 software and screened for genotyping errors before subjecting the data to statistical analysis. Multilocus mating system program (MLTR), described by Ritland (2002), was used to estimate A. senegal mating system, based principally on mixed mating model of Ritland and Jain (1981). This model assumes that (a) there is random mating among individuals (with probability, t, for the outcrossing mating and s = 1 - tm for selfing mating); (b) the maternal genotype does not determine the outcrossing probability; (c) all maternal trees are

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pollinated from a homogenous pollen pool; (d) there is no selection between the time of assay for seedling genotypes and fertilization; and (e) there is independent segregation of alleles at different loci. Single-locus outcrossing rate (ts), multilocus outcrossing rate (tm), mating among relatives (tm - ts), fixation index of maternal parents (Fm), fixation index of the offspring (Fo), correlation of outcrossing rate among progeny arrays (rt) and the correlation of paternity (rp) were calculated using maximum likelihood procedures (Ritland 1996). 95% bootstrap confidence interval was obtained after 1000 re-sampling of individuals within families. The effective number of pollen donors (Nep = 1/rp), or neighborhood size, that contribute to each family was estimated as described by Ritland (1989). We tested for random outcrossing patterns by verifying allelic frequencies of pollen and ovules for heterogeneity by estimating genetic differentiation among families within population, GST (Hedrick 2005). The coefficient of co-ancestry (H) within families for each of the two populations, was calculated as described by Sebbenn (2006);   H ¼ 0:125ð1 þ Fm Þ ð4s þ stm rt Þtm2 1  rp where Fm is the fixation index of the maternal trees and S is the selfing rate (S = 1 - tm). The effective population size within progeny arrays was estimated following Cockerham (1969), from the sample variance in gene frequency as described in Tambarussi et al. (2016): Ne ¼

H

0:5  1F þ 2n o

n1 n

where H is the coefficient of co-ancestry, n is the sample size and FO is the fixation index of the offspring. The number of seed trees (m) necessary to retain a reference effective population size (Ne(r)) of 150 (Lacerda et al. 2008) was calculated as m = Ne(r)/Ne (Sebbenn 2006). The estimate of m is based on three assumptions: (1) seed trees are not related; (2) seed trees do not receive an overlapping pollen pool; (3) seed trees do not mate with each other.

Results Regarding the disturbance indices, Kampi ya Moto population recorded higher population disturbance index (PDI = 53%) than Lake Bogoria population (PDI = 4.1%). Kampi ya Moto showed presence of more cut tree stumps, high presence of grazing livestock, level of seedling browsing, number of new settlements, number of fenced plots, presence of cultivated land and lower density of adult trees, and hence classified as heavily disturbed. Lake Bogoria population showed higher density of adult trees and low PDI value (4.1%), with few charcoal kilns, and no presence of new settlements, fenced plots, or cultivated land (Table 1), and thus, was classified as lightly disturbed. Seed germination per family ranged from 35 to 75%. All the 12 microsatellite loci used in this study were polymorphic and segregated from eight to 20 alleles per loci and no null alleles were detected on all the loci. We found a total of 122 alleles in the two populations, and no allele was exclusive for pollen, ovule or population. Frequencies of pollen alleles were heterogeneous among the maternal individuals for 77% of the loci in Kampi ya Moto population (P \ 0.05) but was homogenous for all the loci in Lake Bogoria population. The single-locus (ts) and multilocus (tm) outcrossing rates for A. senegal maternal trees separately and for both populations are shown in Tables 2 and 3, respectively. The tm

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New Forests Table 1 Population disturbance index (PDI), density of adult trees within the study populations Indicator

Lake Bogoria

Kampi ya Moto

Number of cut tree stumps

12.8

62.5

Number of charcoal kilns

0

8.6

Presence of grazing livestock

0.6

36.5

Level of seedling browsing

15.6

86.2

Number of new settlements

0

56.1

Number of fenced plots

0

56.8

Presence of cultivated land

0

64.6

Population disturbance index (PDI)%

4.1

53

Density (number of adult trees/ha)

414

22

Values given in percentage (%)

Table 2 Mating system indices for the two contrasting populations of Senegalia senegal in Kenya (Lake Bogoria and Kampi ya Moto) Maternal tree

n

Fm

Fo

tm

ts

tm - ts

rp

Nep

Lake Bogoria 1

10

0.036

0.058

1.00

0.88

0.12

0.058

17.24

Lake Bogoria 2

10

0.026

0.075

1.00

0.93

0.07

0.056

17.86

Lake Bogoria 3

11

0.032

0.07

1.00

0.99

0.01

0.053

18.87

Lake Bogoria 4

10

0.026

0.076

1.00

0.88

0.12

0.062

16.13

Lake Bogoria 5

10

0.036

0.096

1.00

0.88

0.12

0.055

18.18

Lake Bogoria 6

11

0.028

0.068

1.00

0.96

0.04

0.052

19.23

Lake Bogoria 7

10

0.038

0.088

1.00

0.93

0.07

0.057

17.54

Lake Bogoria 8

10

0.038

0.061

1.00

0.98

0.02

0.051

19.61

Lake Bogoria 9

10

0.034

0.062

1.00

0.89

0.11

0.054

18.52

Lake Bogoria 10

10

0.046

0.066

1.00

0.94

0.06

0.052

19.23

Kampi ya Moto 1

10

0.033

0.088

0.94

0.82

0.12

0.345

2.90

Kampi ya Moto 2

10

0.035

0.098

0.98

0.83

0.15

0.401

2.49

Kampi ya Moto 3

10

0.034

0.088

0.91

0.79

0.12

0.288

3.47

Kampi ya Moto 4

10

0.035

0.086

0.96

0.87

0.09

0.321

3.12

Kampi ya Moto 5

10

0.034

0.096

0.95

0.88

0.07

0.299

3.34

Kampi ya Moto 6

10

0.026

0.088

0.98

0.82

0.16

0.382

2.62

Kampi ya Moto 7

10

0.03

0.086

0.89

0.83

0.06

0.311

3.22

Kampi ya Moto 8

10

0.025

0.092

0.93

0.81

0.12

0.335

2.99

Kampi ya Moto 9

10

0.032

0.09

0.96

0.84

0.12

0.264

3.79

Kampi ya Moto 10

10

0.026

0.098

0.99

0.84

0.15

0.344

2.91

n family sample size, Fm and Fo are the fixation index of maternal trees and within families, respectively, tm multilocus outcrossing rate, ts single locus outcrossing rates, tm - ts mating among relatives, rp paternity correlation, Nep number of effective pollen donors

estimates were significantly different between the two populations. However, only Kampi ya Moto population showed a mean value significantly different from unity (tm = 0.949; P \ 0.05). Lake Bogoria population showed an exclusive outcrossing mating pattern, with

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New Forests Table 3 Mating system parameters of the two contrasting populations of S senegal in Kenya Parameters

Lake Bogoria

Kampi ya Moto

Maternal tree (offspring)

10 (102)

10 (100)

Multilocus outcrossing rate (tm)

1.000 (0.183)

0.949 (0.004)*

Single locus outcrossing rate (ts)

0.926 (0.079)

0.833 (0.016)*

Mating among relatives (tm - ts)

0.074 (0.373)

0.116 (0.025)*

Selfing (S = 1 - tm)

0

0.167

Correlation of outcrossing rate among progeny arrays (rt)

0.07 (0.026)

0.12 (0.057)

Multilocus paternity correlation (rp)

0.055 (0.439)

Effective number of pollen donors (Nep = 1/rp)

18.182

0.329 (0.762) 3.039

Fixation index in adult trees (Fm)

0.034 (0.081)

0.031 (0.068)

Fixation index in offspring (Fo)

0.072 (0.077)

0.091(0.056)

Coancestry coefficient within progenies (H)

0.136 (0.087)

0.208 (0.039)*

Variance effective size (Ne)

3.57

2.37

Reference effective size (Ne(r))

150

150

Number of seed trees (m)

42

63

Genetic differentiation among families (Gst)

0.013 (0.108)

0.105 (0.027)*

P values are shown in parenthesis * Significantly different at P \ 0.05

100% of the seeds originating from outcross events in all the families (tm = 1.0; P [ 0.05). Generally, all the families revealed high tm values in both populations with low variations among the families (Table 2). The mean multilocus outcrossing rate (tm) was higher than the single locus outcrossing rate (ts) for both populations (Table 3). The mating among relatives (tm - ts) was low and not significantly different from zero in all the families for Lake Bogoria population. However, the value was high and significantly different from zero for Kampi ya Moto population (Table 3). The average fixation index of the maternal trees (Fm) and offspring (Fo) for both populations and families were not significantly different from zero, showing absence of inbreeding (Tables 2, 3). The correlation of paternity (rp) and correlation of outcrossing rate among progeny arrays (rt) differed between the two populations. For Lake Bogoria population, the rp estimate was low (rp = 0.055). However, for Kampi ya Moto population, paternity correlation (rp = 0.329) was high, suggesting that many seeds within families are full-sibs. The low values of rt in both populations, 0.07 and 0.12, for Lake Bogoria and Kampi ya Moto, respectively (Table 3), agree with the limited variations found in the outcrossing rates among progenies within the two populations (Table 2). The effective number of pollen donors (1/rp) was about 18 in Lake Bogoria population, which was six times higher than that found in Kampi ya Moto population (Nep = 3). High genetic differentiation among families was found in Kampi ya Moto (Gst = 0.105; P \ 0.05) compared to Lake Bogoria (Gst = 0.013; P [ 0.05) as shown in Table 3. The coefficient of coancestry within progeny from Kampi ya Moto population (H = 0.208) was higher and closer to the value expected for non-randomly mating population (many full-sib families, H = 0.25), when compared to Lake Bogoria population that showed a value (H = 0.136) closer to that expected for a panmictic and randomly

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mating population (mainly half-sib families, H = 0.125). The variance effective size was significantly higher for Lake Bogoria population (Ne = 3.57) and closer to the maximum value that a family can achieve (Ne = 4), when compared to Kampi ya Moto population (Ne = 2.37). Consequently, the number of seed trees required for seed collection (m) to retain effective population size of 150 was significantly higher in Kampi ya Moto population (m = 63) than in Lake Bogoria population (m = 42).

Discussion The 12 microsatellite markers used in this study did not reveal presence of null alleles, and showed high allelic diversity in both populations. The characteristics of the markers showed their reliability for undertaking mating system studies. Importantly, this is the first report to use such a large battery of microsatellite loci in the estimation of mating system of an African Acacia species. Acacia senegal displayed a predominantly outcrossing mating pattern in both populations. The multilocus outcrossing rates determined for Lake Bogoria populations was equal to unity (1.0), which is an indication that this population was exclusively outcrossing. However, this value was significantly higher than the outcrossing rate estimated for Kampi ya Moto population, which we classified as heavily disturbed based on PDI. Nonetheless, the outcrossing rate estimates in both populations were consistent with the results reported so far for other tropical tree species (Khasa et al. 1993; Boshier et al. 1995; Obunga 1995; Liengsiri et al. 1998; Lee et al. 2000; Collevatti et al. 2001; Casiva et al. 2004; Ward et al. 2005; Diallo et al. 2015). Our study also corroborated the earlier result of mating system study by Obunga (1995), which used controlled pollination test to determine the levels of seed set when pollen come from different sources, and concluded that A. senegal is an outbreeding specie with a predominantly outcrossing mating pattern. The predominantly outcrossing mating pattern found in the present study can be attributed to the presence of some level of genetically induced self-incompatibility in A. senegal. The species has flower development process, which is likely to present mechanism to avoid selfing. In fact, all members of the formally Aculeiferum subfamily complex that included A. senegal, have protandrous flowers (stamens that mature before carpels), a temporal mechanism that favors outcrossing, although variation in outcrossing rates among populations was reported by Tandon and Shivanna (2001) for some species in this complex. The anatomic structure of A. senegal flowers may also present physical barriers, isolating the stigma from the anthers, promoting pre-zygotic incompatibility (Obunga 1995; Tybirk 1997). Furthermore, late self-incompatibility mechanisms that may be operating inside the embryo sac, through seed abortion has also been reported by Obunga (1995) and Diallo et al. (1997). Indeed, Diallo et al. (1997) found negligible fruit set in artificially self-pollinated flowers of A. senegal, demonstrating the significance of outcrossing mating pattern to the species reproduction system. Despite high outcrossing rates reported for both the A. senegal populations, Kampi ya Moto population recorded a lower outcrossing rate than Lake Bogoria population. Although the two populations underwent human interference, Kampi ya Moto showed low density of adult trees and higher PDI compared to Lake Bogoria population. This finding suggested that the reduction in adult tree density and heightened man-made disturbance observed in the population compared to Lake Bogoria might have induced some level of selfing or mating among relatives. As suggested by White et al. (2007), variation in stand

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density generally influences the population of flowering trees and ultimately the outcrossing rates and probably promotes mating among close relatives, where seed dispersal occurs in short distances. Similar result was reported for Pterocarpus macrocarpus by Liengsiri et al. (1998), suggesting that habitat disturbance and probably the distribution and density of flowering trees influenced the variations in outcrossing rates among populations of the species. In addition, Murawski and Hamrick (1992) also showed a positive relationship between the number of flowering plants and the outcrossing rates for Cavanillesia platanifolia. Generally, population with high adult tree density, like Lake Bogoria, tend to have high probability of one receptive tree receiving pollen from many pollen donors and, hence, greater chances for outcrossing (Ward et al. 2005). Indeed, tree density is among the critical demographic variables influencing mating pattern of tree species, as well as the within and among population genetic differentiation (White et al. 2007; Davies et al. 2015). Our study suggests the presence of strong relationship between tree density and biparental inbreeding. Kampi ya Moto population, which had low adult tree density, showed higher and significant biparental inbreeding values compared to the Lake Bogoria, which had higher density of adult tree. Generally, as the distance between stands or individual trees increases in species with bisexual flowering events such as A. senegal, high proportions of the available pollen are usually from self or close relatives, leading to high rates of selfing or correlated mating (White et al. 2007). Correlated mating generally occur where closely related trees grow in clusters and undergoes localized mating patterns (Sun and Ritland 1998; Kikuchi et al. 2015). This can be evidenced by the reported presence of significant genetic differentiation among families within Kampi ya Moto population. The present result was also supported by our recent finding on A. senegal that found significant deviation from Hardy–Weinberg Equilibrium (HWE) in Kampi ya Moto population and suggested genetic sub-structuring and nonrandom mating pattern within the population (Omondi et al. 2016a). The clustering of related individuals in this population may have been enhanced by short seed dispersal distance, most likely by wind, since the ungulate dispersal is relatively low in this area. Similar result was reported by Suarez-Gonzalez (2011) for chokecherry species (Prunus virginiana), whose seeds are also wind dispersed. Our findings also agree with other studies that have reported higher biparental inbreeding in disturbed and fragmented habitats (Mimura et al. 2009; Kikuchi et al. 2015 and references therein). The biparental inbreeding observed in the current study may also be due to assortative mating patterns, where flowering synchrony occurs between genetically related trees (Omondi et al. 2016b). However, this hypothesis can only be tested when detailed demographic, genetic and flowering phenology studies are undertaken together with the mating system (Lemes et al. 2007). Several factors could account for the differences in allelic frequencies found between the pollen and ovules in Kampi ya Moto population. This may include non-randomness of the outcrossing events as well as some pollen immigration from outside the population as reported by Lee et al. (2000). The higher correlated paternity observed for Kampi ya Moto population (rp = 0.329) compared to Lake Bogoria population (rp = 0.055), corroborated the theory of nonrandom mating pattern. This means that mating individuals are more closely related or less closely related than those drawn by chance from a random mating population. The result further justified that more full-sib offspring could be found in Kampi ya Moto population (H = 0.233, equivalent to about 23% of the offspring being full-sibs). However, the majority (77% [100–23]) of the offspring were half-sibs, probably derived from random mating. Indeed, the coefficient of co-ancestry within progeny for Kampi ya Moto population was almost the value of full-sib families (0.25). This suggested the

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absence of self-fertilization but the presence of limited random mating within this population. These results also indicated that few individuals (only about 3 effective pollen donors) contributed to seed production (see Sun and Ritland 1998). Furthermore, correlation of paternity so far reported for tropical tree species are similar to the ones reported in the present study, with more prevalence in disturbed habitats (Seoane et al. 2001; Sebbenn et al. 2001; Alves et al. 2003). Foraging patterns of pollinators usually affect mating patterns in trees (Lander et al. 2011). Although not tested in the present study, honey bees are the most frequent flower visitor and among the listed pollinator of the A. senegal (Obunga 1995; Tandon and Shivanna 2001). Generally, honey bees are known to visit few trees and spend time on several flowers on one or several inflorescences of the same tree before moving to the neighboring trees and may come back to the same tree (Sun and Ritland 1998). This foraging behavior allows exchange of pollen between only few trees. Therefore, with the reduced adult tree density in Kampi ya Moto population, interplant distance increases, and probably may lead to the likelihood of increased selfing or near neighborhood mating (Feres et al. 2012). The observation is supported by the low numbers of effective pollen donors, high proportions of likely full-sibs and high level of mating among relatives found in Kampi ya Moto population. Generally, selfing or mating among relatives increase the frequency of alleles identical by descent, thus decreasing the variance effective size, as observed for Kampi ya Moto population. This affect the number of seed trees for seed collection (m), to retain progeny arrays with a reliable effective size (usually 150). Despite Kampi ya Moto population being more disturbed than Lake Bogoria, it should still be considered in the conservation plan of the species and tree present in the population can serve as seed sources. Seed for conservation and breeding programs can be collected from 63 to 42 seed trees in Kampi ya Moto and Lake Bogoria populations, respectively. The present study reaffirmed the long held assumption of predominant outcrossing mating system for A. senegal, and also highlighted that mating system indices such as tm, ts and H varied among environmental contexts. The variations can be attributed to differences in number of pollen sources within the populations (density of adult trees). For genetic conservation programs and seed collection for artificial plantation establishment, variations in outcrossing rates, correlation of paternity, selfing rate and fixation index of progeny and maternal trees should be considered, because they affect the variance effective size of populations. For rehabilitation of disturbed populations of A. senegal, enrichment planting should be undertaken with materials collected outside Kampi ya Moto population to prevent inbreeding depression due to possibility of mating among close relatives. We also found that Ne and m varied between populations, but even the most disturbed one (Kampi ya Moto) may still contribute as seed trees for conservation plans. Moreover, we recommended that seed collection from the two populations for establishment of artificial plantation and enrichment planting in degraded sites should be undertaken from at least 63 and 42 trees in Kampi ya Moto and Lake Bogoria populations respectively. Acknowledgements This study was funded by Kenya Forestry Research Institute (KEFRI) and the International Foundation for Science (IFS), Stockholm, Sweden, through a grant to Stephen F. Omondi Grant No. D5452-1. Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery grant to Prof. Damase P. Khasa towards the study is acknowledged. We are grateful to Biotechnology Laboratory staff of KEFRI for helping during field sampling and laboratory analyses.

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New Forests Compliance with ethical standards Conflict of interest The authors declare that they have no conflict of interest.

References Aguilar R, Quesada M, Ashworth L, Herrerias-Diego Y, Lobo J (2008) Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches. Mol Ecol 17:5177–5188. doi:10.1111/j.1365-294X.2008.03971.x Alves RM, Artero AS, Sebbenn AM, Figueira A (2003) Mating system in natural populations of Theobroma grandiflorum (Willd. ex. Spreng.) Schum., by microsatellite markers. Genet Mol Biol 26:373–379. Mol Ecol 17: 5177–5188. doi:10.1590/S1415-4757200300030002 Baringo County Government (2014) Annual development plan 2015/16. Government printers, Nairobi Beardmore J (1983) Extinction, survival, and genetic variation. In: Schonewald-Cox CM, Chambers SM, MacBryde F, Thomas L (eds) Genetics and conservation: a reference for managing wild animal and plant populations. Benjamin/Cummings, Menlo Park, pp 125–151 Boshier DH, Chase MR, Bawa KS (1995) Population genetics of Cordia alliodora (Boraginaceae), a Neotropical tree, mating system. Am J Bot 82:476–483 Casiva P, Vilardi J, Cialdella A, Saidman B (2004) Mating system and population structure of Acacia aroma and A. macracantha (Fabaceae). Am J Bot 91:58–64. doi:10.3732/ajb.91.1.52 Chikamai BN, Odera JA (2002) Commercial plant gums and resins in Kenya. Nairobi, Kenya Cockerham CC (1969) Variance of gene frequencies. Evolution 23:72–84 Collevatti RG, Grattapaglia D, Hay JD (2001) High resolution microsatellite based analysis of the mating system allows the detection of significant bi-parental inbreeding in Caryocar brasiliense, an endangered tropical tree species. Heredity 86:60–67. doi:10.1046/j.1365-2540.2001.00801 Davies SJ, Cavers S, Finegan B, White A, Breed MF, Lowe AJ (2015) Pollen flow in fragmented landscapes maintains genetic diversity following stand-replacing disturbance in a neotropical pioneer tree, Vochysia ferruginea Mart. Heredity 115:125–129 de-Lucas AI, Robledo-Arnuncio JJ, Hidalgo E, González-Martı́nez SC (2008) Mating system and pollen gene flow in Mediterranean maritime pine. Heredity 100:390–399. doi:10.1038/sj.hdy.6801090 Diallo I, Samb PI, Gaye A, Sall PN, Duhoux E, Ba AT (1997) Floral biology and pollination in Acacia senegal (L.) Willd. Biologie florale et pollinisation chez Acacia senegal (L.) Willd. Bot Lett 144(1):73–82. doi:10.1080/12538078.1997.10515755 Diallo AM, Nielsen LR, Hansen JK, Ræbild A, Kjær ED (2015) Study of quantitative genetics of gum arabic production complicated by variability in ploidy level of Acacia senegal (L.) Willd. Tree Genet Genomes 11:80–92. doi:10.1007/s11295-015-0902 Dick CW, Etchelecu G, Usterlitz FA (2003) Pollen dispersal of tropical trees (Dinizia excelsa: Fabaceae) by native insects and African honeybees in pristine and fragmented Amazonian rainforest. Mol Ecol 12:753–764. doi:10.1046/j.1365-294X.2003.01760 Duminil J, Abessolo MDT, Bourobou DN, Doucet J-L, Loo J, Hardy OJ (2016) High selfing rate, limited pollen dispersal and inbreeding depression in the emblematic African rain forest tree Baillonella toxisperma—management implications. For Ecol Manag 379:20–29 Eckert CG, Kalisz S, Geber MA, Sargent R, Elle E, Cheptou PO, Goodwillie C, Johnston MO, Kelly JK, Moeller DA, Porcher E, Ree RH, Vallejo-Marı́n M, Winn AA (2010) Plant mating systems in a changing world. Trends Ecol Evol 25:35–43. doi:10.1016/j.tree.2009.06.013 Ellstrand NC, Ellam RD (1993) Population genetic consequences of small population size: implications for plant conservation. Annu Rev Ecol Syst 24:217–242. doi:10.1146/annurev.es.24.110193.001245 Fagg CW, Allison GE (2004) Acacia senegal and gum arabic trade: monographs and annotated bibliography. Tropical forestry papers. No. 42. Oxford Forestry Institute, Oxford, UK Feres JM, Sebbenn AM, Guidugli MC, Mestriner MA, Moraes MLT, Alzate–Marin AL (2012) Mating system parameters at hierarchical levels of fruits, individuals and populations in the Brazilian insect— pollinated tropical tree, Tabebuia roseo–alba (Bignoniaceae). Conserv Genet 13:393–405. doi:10. 1007/s10592-011-0292-z Franceschinelli EV, Bawa KS (2000) The effect of ecological factors on the mating system of a South American shrub species (Helicteres brevispira). Heredity 84:116–123. doi:10.1046/j.1365-2540.2000. 00636.x Frankham R, Ballou JD, Eldridge MDB, Lacy RC, Ralls K, Dudash MR, Fenster CB (2011) Predicting the probability of outbreeding depression. Conserv Biol 25:465–475. doi:10.1111/j.1523-1739.2011. 01662.x

123


New Forests Fuchs E, Lobo JA, Quesada M (2003) Effects of forest fragmentation and flowering phenology on the reproductive success and mating patterns on the tropical dry forest tree, Pachira quinata (Bombacaceae). Conserv Biol 17:149–157. doi:10.1046/j.1523-1739.2003.01140.x Hall P, Walker S, Bawa K (1996) Effect of forest fragmentation on genetic diversity and mating system in a tropical tree, Pithecellobium elegans. Conserv Biol 10:757–768. doi:10.1046/j.1523-1739.1996. 10030757.x Hanaoka S, Omondi SF, Machua J (2013) Basic molecular techniques for tree breeding—experimental protocols. Sankeisha co. ltd, Aichi Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 8:1633–1638 Jacquemyn H, De Meester L, Jongejans E, Honnay O (2012) Evolutionary changes in plant reproductive traits following habitat fragmentation and their consequences for population fitness. J Ecol 100:76–87. doi:10.1111/j.1365-2745.2011.01919.x Karasawa MM, Vencovsky R, Silva CM, Zucchi MI, Oliveira GC, Veasey EA (2007) Mating system of Brazilian Oryza glumaepatula populations studied with microsatellite markers. Ann Bot 99:245–253. doi:10.1093/aob/mcl248 Khasa DP, Cheliak WM, Bousquet J (1993) Mating system of Racosperma auriculiforme in a seed production area in Zaire. Can J Bot 71:779–785. doi:10.1139/b93-089 Kikuchi S, Shibata M, Tanaka H (2015) Effects of forest fragmentation on the mating system of a cooltemperate heterodichogamous tree Acer mono. Glob Ecol Conserv 3(2015):789–801. doi:10.1016/j. gecco.2015.04.005 Lacerda EBL, Kanashiro M, Sebbenn AM (2008) Long-pollen movement and deviation of random mating in a low-density continuous population of Hymenaea courbaril in the Brazilian Amazon. Biotropica 40:462–470 Lander TA, Bebber DP, Choy CTL, Harris SA, Boshier DH (2011) The circe principle explains how resource-rich land can waylay pollinators in fragmented landscapes. Curr Biol 21(15):1302–1307 Lee SL, Wickneswari R, Mahani MC, Zakri AH (2000) Mating system parameters in a tropical tree species, Shorea leprosula Miq. (Dipterocarpaceae), from Malaysian lowland dipterocarp forest. Biotropica 32(4):693–702. doi:10.1111/j.1744-7429.2000.tb00517.x Lemes MR, Grattapaglia D, Grogan J, Proctor J, Gribel R (2007) Flexible mating system in a logged population of Swietenia macrophylla Kind (Meliaceae): implication for the management of threatened neotropical tree species. Plant Ecol 192:169–179. doi:10.1007/s11258-007-9322-9 Liengsiri C, Boyle TJB, Yeh FC (1998) Mating system in Pterocarpus macrocarpus Kurz in Thailand. J Hered 89:216–221. doi:10.1093/jhered/89.3.216 Lowe AJ, Boshier D, Ward M, Bacles CFE, Navarro C (2005) Genetic resource impacts of habitat loss and degradation; reconciling empirical evidence and predicted theory for Neotropical trees. Heredity 95:255–273. doi:10.1038/sj.hdy.6800725 Millar M, Coates D, Byrne M (2014) Extensive long-distance pollen dispersal and highly outcrossed mating in historically small and disjunct populations of Acacia woodmaniorum (Fabaceae), a rare banded iron formation endemic. Ann Bot 114(5):961–971. doi:10.1093/aob/mcu167 Mimura M, Barbour RC, Potts BM (2009) Comparison of contemporary mating patterns in continuous and fragmented Eucalyptus globulus native forests. Mol Ecol 18:4180–4192. doi:10.1111/j.1365-294X. 2009.04350.x Murawski DA, Hamrick JL (1992) The mating systems of Cavanillesia platanifolia under extremes of flowering-tree density: a test of predictions. Biotropica 24:99–101. doi:10.2307/2388478 Obunga EO (1995) A study of genetic systems of four African species of Acacia. Dissertation, University of Sussex Omondi FS, Kireger E, Dangasuk GO, Chikamai B, Odee DW, Cavers S, Khasa DP (2010) Genetic diversity and population structure of Acacia senegal (L) Willd. in Kenya. Trop Plant Biol 3:59–70. doi:10.1007/ s12042-009-9037-2 Omondi SF, Ongamo GO, Kanya JI, Odee DW, Khasa DP (2016a) Genetic consequences of anthropogenic disturbances and population fragmentation in Acacia senegal. Conserv Genet. doi:10.1007/s10592016-0854-1 Omondi SF, Ongamo GO, Kanya JI, Odee DW and Khasa DP (2016b) Synchrony in leafing, flowering and fruiting phenology of Senegalia senegal within Lake Baringo woodland, Kenya: Implication for conservation and tree improvement. Int J For Res 2016, Article ID 6904834 Ritland K (1989) Correlated matings in the partial selfer Mimulus guttatus. Evolution 43:848–859 Ritland K (1996) Multilocus mating system program (MLTR). Version1.1. Department of Botany, University of Toronto, Toronto Ritland K (2002) Extensions of models for the estimation of mating systems using n independent loci. Heredity 88:221–228. doi:10.1038/sj.hdy.6800029

123


New Forests Ritland K, Jain SK (1981) A model for estimation of outcrossing rate and gene frequencies using independent loci. Heredity 47:35–52. doi:10.1038/hdy.1981.57 Sebbenn AM (2006) Sistemas de reprodução em espécies tropicais e suas implicações para a seleção de árvores matrizes para reflorestamentos ambientais. In: Higa AR, Silva LD (eds) Pomar de sementes de espécies florestais nativas. FUPEF do Paraná, Curitiba, pp 93–138 Sebbenn AM, Seoane CEC, Kageyama PY, Lacerta CM (2001) Estrutura genética em populações de Tabebuia cassiroides: implicações para o manejo florestal e conservação genética. Revista do Instituto Florestal 13:99–111 Seoane CEC, Sebbenn AM, Kageyama PY (2001) Sistema reprodutivo em populações de Esenbeckia leiocarpa. Revista do Instituto Florestal 13:21–28 Suarez-Gonzalez A (2011) Reproductive and genetic consequences of fragmentation in chokecherry (Prunus virginiana L.). Dissertation, University of Winnipeg Sun M, Ritland K (1998) Mating system of yellow starthistle (Centaurea solstitialis), a successful colonizer in North America. Heredity 80:225–232. doi:10.1046/j.1365-2540.1998.00290.x Tamaki I, Ishida K, Setsuko S, Tomaru N (2009) Inter-population variation in mating system and late-stage inbreeding depression in Magnolia stellata. Mol Ecol 18:2365–2374. doi:10.1111/j.1365-294X.2009. 04195.x Tambarussi EV, Boshier DH, Vencovsky R, Freitas MLM, Di-Dio OJ, Sebbenn AM (2016) Several small: how inbreeding affects conservation of Cariniana legalis Mart. Kuntze (Lecythidaceae) the Brazilian Atlantic Forest’s largest tree. Int For Rev 18(4):502–510 Tandon R, Shivanna KR (2001) Pollination biology and breeding system of Acacia senegal. Bot J Linean Soc 135:251–262. doi:10.1111/j.1095-8339.2001.tb01094.x Tybirk K (1997) Reproductive biology and evolution of the genus Acacia. Bull Int Gr Study Mimosoideae 20:45–53 Ward M, Dick CW, Gribel R, Lowe AJ (2005) To self, or not to self. A review of outcrossing and pollenmediated gene flow in neotropical trees. Heredity 95:246–254. doi:10.1038/sj.hdy.6800712 Wekesa C, Makenzi PM, Chikamai BN, Luvanda AM, Muga MO (2010) Traditional ecological knowledge associated with Acacia senegal (gum arabic tree) management and gum arabic production in northern Kenya. Int For Rev 12(3):240–246 White TL, Adams WT, Neale DB (2007) Forest genetics. CAB international, Oxfordshire Young AG, Boyle T, Brown ADH (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418. doi:10.1016/0169-5347(96)10045-8

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