Reproduction

The way in which a species reproduces can have a strong influence on gene flow. Morjan and Rieseberg (2004) obtained estimates of gene flow from the literature by reviewing all relevant studies published in the journal Molecular Ecology between 1992 and 2002. They found a significant relationship between gene flow and the method of reproduction in both plants and animals. In both groups, populations that reproduce by either outcrossing or a mixture of outcrossing and selfing/cloning generally showed lower levels of differentiation and higher levels of gene flow than populations that reproduced solely by selfing/clonal reproduction (Table 4.7).

The relationship between reproduction and dispersal has been particularly well studied in plants, where it can be explained largely by different mechanisms of pollen dispersal. Outcrossing plants are either wind- or animal-pollinated, and therefore their pollen has the potential to travel relatively long distances. Plants that self-fertilize, on the other hand, generally lack any mechanism for pollen dispersal, and therefore pollen-mediated gene flow is low in these species. Both

Table 4.7 Estimates of gene flow in plants and animals, grouped according to reproductive mode (Morjan and Rieseberg, 2004). In each category, n refers to the number of studies that were included in the comparisons. Note that FST and Nem values in this table are not directly comparable as they are based on slightly different sets of comparisons

Table 4.7 Estimates of gene flow in plants and animals, grouped according to reproductive mode (Morjan and Rieseberg, 2004). In each category, n refers to the number of studies that were included in the comparisons. Note that FST and Nem values in this table are not directly comparable as they are based on slightly different sets of comparisons

fst

Nem

n

Mean

Median

n

Mean

Median

Plants

Outcrossing

74

0.29

0.14

73

1.38

1.47

Mixed

174

0.30

0.18

170

2.99

1.17

Selfing or clonal

22

0.43

0.36

22

0.43

0.45

Animals

Outcrossing

216

0.22

0.11

219

4.67

2.09

Mixed

14

0.40

0.16

13

7.55

1.50

Selfing or clonal

11

0.24

0.22

11

2.99

0.90

outcrossing and self-fertilizing species produce seeds, but seeds generally travel shorter distances than pollen. This has been demonstrated by numerous studies that estimated population differentiation and gene flow from at least two of the three plant genomes (nuclear, plastid and mitochondria) having different patterns of inheritance (Chapter 2). For any given species we can compare estimates of FST (or analogue) that have been calculated from nuclear and organelle data to obtain a pollen/seed migration ratio (Ennos, 1994; Hamilton and Miller, 2002). A recent review of 93 studies calculated a mean pollen/seed gene flow ratio of 17, which shows that pollen is the main agent of gene flow in many plants (Petit et al., 2005; see also Table 4.8). As a result, pollen dispersal mechanisms play an extremely

Table 4.8 Some examples of the estimated ratios of pollen-mediated gene flow to seed-mediated gene flow. For each species the ratio was based on a comparison of FST values (or analogue) that were calculated from two genomes that are inherited in different ways, typically nuclear versus plastid or mitochondrial data. A ratio of >0 means that pollen-mediated gene flow exceeds seed-mediated gene flow; the prevalence of this was reported recently in a review of 93 different studies in which the authors calculated a mean pollen/seed gene flow ratio of 17 (Petit et al., 2005)

Species Pollen/seed gene flow Reference

Table 4.8 Some examples of the estimated ratios of pollen-mediated gene flow to seed-mediated gene flow. For each species the ratio was based on a comparison of FST values (or analogue) that were calculated from two genomes that are inherited in different ways, typically nuclear versus plastid or mitochondrial data. A ratio of >0 means that pollen-mediated gene flow exceeds seed-mediated gene flow; the prevalence of this was reported recently in a review of 93 different studies in which the authors calculated a mean pollen/seed gene flow ratio of 17 (Petit et al., 2005)

Species Pollen/seed gene flow Reference

Oak (Quercus petraea)

500

El Mousadik and Petit (1996)

Oak (Q. robur) complex

286

El Mousadik and Petit (1996)

A tropical canopy tree,

200

Hamilton and Miller (2002)

Corythophora alta

Lodgepole pine (Pinus contorta)

28

Ennos (1994)

White campion (Silene alba)

3.4 (large scale)-

McCauley (1997)

124 (fine scale)

Wild barley (Hordeum spontaneum)

4

Ennos (1994)

Rowan tree (Sorbus torminalis)

2.21

Oddou-Muratorio et al. (2001)

Helleborine orchid, Epipactis helleborine

1.43

Squirrell et al. (2001)

A) Seed dispersal

B) Pollen dispersal

A) Seed dispersal

B) Pollen dispersal

Figure 4.7 The mean GST values (with error bars) between populations of plants with (A) different seed dispersal mechanisms, none of which are significantly different from each other, and (B) different pollen dispersal mechanisms, all of which are significantly different from each other. Adapted from Hamrick and Godt (1990)

Figure 4.7 The mean GST values (with error bars) between populations of plants with (A) different seed dispersal mechanisms, none of which are significantly different from each other, and (B) different pollen dispersal mechanisms, all of which are significantly different from each other. Adapted from Hamrick and Godt (1990)

important role in determining the genetic structure among plant populations (Figure 4.7).

Fragmented habitats and metapopulations

Another factor that influences gene flow is the distribution of suitable habitats across the landscape. Species that live in temporary habitats may frequently disperse between sites, for example the coastal dune spider (Geolycosa pikei) that lives in ephemeral inlets showed very little genetic differentiation among ten seemingly isolated populations (Boulton, Ramirez and Blair, 1998). On the other hand, fairy shrimp (Branchinecta sandiegonensis) populations that inhabit ephemeral pools on coastal mesas in San Diego County, USA, showed substantial levels of genetic differentiation (FST typically >0.25) that could be attributable to low gene flow (Davies, Simovich and Hathaway, 1997). It therefore seems that patchy or fragmented habitats lead to high gene flow in some species and low gene flow in others, although of course some gene flow is necessary for the survival of species that inhabit only ephemeral sites.

If a species lives in a fragmented habitat and regularly disperses between suitable sites it may form what is known as a metapopulation. The concept of a metapopulation dates back to the 1930s, although the actual term is attributable to Levins (1969) who presented an explicit model of a metapopulation. Levins' model, which we know now as a classical metapopulation, refers to a 'population of populations' that exist in a balance between extinction and recolonization, and are linked to one another by ongoing dispersal and gene flow. Classical metapo-pulations in the wild have been documented in a number of species, including three species in the freshwater zooplankton genus Daphnia, which in one study were found to be distributed across 507 rock pools on 16 islands. In any given year, the three species occupied between 5.6 and 17.8 per cent of the pools. Over a 17-year period, average yearly extinction rates of individual rock pools were around 20 per cent, and these were more or less balanced by the number of colonizations (Pajunen and Pajunen, 2003).

Metapopulations also have been identified within several species of the plant genus Silene. The high genetic differentiation (mean FST = 0.287) between subpopulations of a riparian metapopulation of S. tatarica in Finland suggested relatively low levels of gene flow (Tero et al., 2003). In contrast, much lower levels of genetic differentiation (mean FST = 0.007) suggested substantially higher levels of gene flow in the tundra species S. acaulis (Gehring and Delph, 1999), once again reflecting a lack of consistency in the extent to which subdivided populations exchange immigrants. We may conclude from these previous examples that the subdivision of habitats is not a useful prediction of dispersal, possibly because it is a phenomenon that transcends a host of ecological and geographical variables. However, we must also bear in mind that populations that are regularly experiencing extinctions and recolonizations are unlikely to have reached equilibrium, in which case we must be particularly cautious in using FST values to infer indirect estimates of gene flow.

As the concept of a metapopulation has become more commonplace in the literature, several variations have emerged. A slight modification of the original concept, which required all subpopulations to have an equal probability of going extinct at any given time, is the island-mainland model. This describes a metapopulation in which a small number of regional populations (mainlands) remain relatively stable over time and act as sources of (re)colonizers for new populations (islands). More recently, the term has often been adapted broadly to refer simply to a series of conspecific populations that are connected to one another by dispersal. In accordance with this modified view, in which localized extinctions are not necessarily a prerequisite, a number of alternative metapopulation models have been created. There is, however, some debate in the literature over whether these simply represent a series of subdivided populations.

The process of repeated extinctions and recolonizations can affect the genetic structure of a metapopulation in different ways. Extinctions and recolonizations will often be accompanied by population bottlenecks, which, as we know from Chapter 3, lead to reduced effective population size (Ne), accelerated genetic drift, and depleted genetic variation. The Ne will be substantially reduced if all extant populations within a metapopulation descended relatively recently from a single ancestral population (Figure 4.8). Extinctions and recolonizations will also affect the extent to which populations are genetically differentiated from one another. Depending upon the balance between genetic drift and gene flow, differentiation

Subpopulations

Subpopulations

Figure 4.8 An original metapopulation consisting of six subpopulations undergoes a series of extinctions and recolonizations. Shaded circles represent occupied sites and white circles represent extinct populations. Lines between circles indicate the source of colonizing individuals. In the most recent time period, the metapopulation consists of four subpopulations (2, 3, 4 and 5). All of these have descended recently from individuals that dispersed from a single subpopulation (subpopulation 3) and therefore the overall Ne will be substantially lower than the Nc

Figure 4.8 An original metapopulation consisting of six subpopulations undergoes a series of extinctions and recolonizations. Shaded circles represent occupied sites and white circles represent extinct populations. Lines between circles indicate the source of colonizing individuals. In the most recent time period, the metapopulation consists of four subpopulations (2, 3, 4 and 5). All of these have descended recently from individuals that dispersed from a single subpopulation (subpopulation 3) and therefore the overall Ne will be substantially lower than the Nc among local populations may be enhanced if the founding of a new population is accompanied by a pronounced bottleneck, or diminished if gene flow remains high.

It is becoming increasingly important for us to understand the genetics of metapopulations, because habitat fragmentation is transforming a growing number of formerly continuous populations into subdivided units with varying degrees of connectivity. Some of the potential effects of habitat fragmentation were illustrated by a couple of studies that compared two sets of populations of the regal fritillary butterfly (Speyeria idalia). One set of populations was located in relatively continuous prairie and farmland habitat (Great Plains populations), whereas the other set was located in habitat that has been fragmented for approximately 150 years (Midwestern populations). The first study, which was based on mtDNA data, revealed little genetic structure among either the Great Plains or Midwestern populations, thereby suggesting that habitat fragmentation had little effect on population differentiation (Williams, 2002). However the second study, based on microsatellite data, revealed higher levels of among-population genetic differentiation and lower levels of gene flow and genetic diversity in the Midwestern populations compared with the continuous Great Plains populations (Williams, Brawn and Paige, 2003). Unfortunately the reduction of dispersal and genetic variation is a fairly common result of habitat fragmentation, making this a frequent matter of concern in conservation genetics. The regal fritillary butterfly studies also remind us how important it is to choose the correct molecular marker when evaluating gene flow and population differentiation.

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