Reproduction

No discussion on the factors that influence genetic diversity is complete without a reference to mode of reproduction. Sexual reproduction has long been viewed as something of a paradox because it predominates within multicellular eukaryotic taxa and yet entails a cost. In most sexual species half of the offspring produced are male, whereas an asexual female will produce only female offspring. Males are costly because their only contribution to the next generation is the fertilization of females. Sexual females therefore have a reduction in fitness compared with asexual females because they pass on only 50 per cent of their genes to each offspring and, because they produce both females and males, their offspring multiply at half the rate of clonal offspring. This result is often expressed as the 'twofold cost of sex' (Maynard Smith, 1978). There must be some advantage, therefore, that can explain the predominance of sex, and the most commonly cited explanation is recombination, which continuously generates novel genotypes that have the potential to adapt to changing environments. This rapid generation of genetic diversity through recombination means that sexually reproducing populations usually have higher levels of genetic diversity than asexual populations (see also Box 3.5).

Comparisons between the genetic diversity of sexual and asexual populations are most reliable when they involve a single species because this reduces the potentially confounding effects that variables other than reproduction may have on genetic variation. One example of this is the aphid Sitobion avenae, which tends to reproduce sexually in areas of Europe that have harsh winters, because the sexually produced eggs can survive low temperatures. In milder areas, parthenogenetic lineages predominate, because adults can survive the winters and have the advantage of high reproductive output. A microsatellite-based comparison between largely asexual populations in western France and sexual populations in Romania showed that the Romanian population had much higher genetic diversity than the French population -- 94 per cent of aphids sampled in Romania had unique genotypes compared with only 28 per cent in France (Papura et al., 2003). The low diversity in France was largely attributable to two dominant genotypes that were found in more than 60 per cent of samples.

Although relatively low levels of genetic diversity have been found in many asexually reproducing populations, it is important to note that not all asexual

Table 3.8 Average heterozygosity values in plants that are grouped according to their mode of reproduction. Calculations are based on RAPD and microsatellite data and n refers to the number of studies included in each category. Numbers within a column are significantly different from one another if they are denoted by different letters. Adapted from Nybom (2004) and references therein

RAPD data Microsatellite data

Table 3.8 Average heterozygosity values in plants that are grouped according to their mode of reproduction. Calculations are based on RAPD and microsatellite data and n refers to the number of studies included in each category. Numbers within a column are significantly different from one another if they are denoted by different letters. Adapted from Nybom (2004) and references therein

RAPD data Microsatellite data

Mode of reproduction

n

He

n

He

n

Ho

Selfing"

10

0.12b

15

0.41b

4

0.05b

Mixed (selfing and outcrossing)

0.18b

8

15

0.60c

13

0.51c

Outcrossing

38

0.27c

71

0.65c

60

0.63d

aSelfing refers to the practice of self-fertilization.

aSelfing refers to the practice of self-fertilization.

populations are genetically depauperate. Seven microsatellite loci revealed a mean of 6.6 alleles per locus and an average He of 0.60 in asexual populations of the aphid Rhopalosiphum padi, an appreciable level of diversity that was nevertheless lower than that found in sexual populations, which had a mean of 11.3 alleles per locus and an average He of 0.642 (Delmotte et al., 2002). In flowering plants, a survey of 653 studies of allozyme variation showed no significant difference between the mean level of gene diversity within populations of sexually reproducing plants (0.114) compared with populations having a mixed (sexual and asexual) reproductive mode (0.103) (Hamrick and Godt, 1990). However, this finding may be an artefact of relatively invariant markers, because a later review of studies based on RAPD and microsatellite data revealed overall higher levels of genetic diversity in outcrossing plants (Nybom, 2004; Table 3.8).

Box 3.5 Hybridization and genetic diversity

Another aspect of reproduction that can influence genetic diversity is hybridization. Interspecific hybridization can result in the transfer of genes, or even entire genomes, from one species to another. Provided that there are no fitness costs associated with these episodes of genetic introgression (and there often are), hybridization can increase the genetic diversity of populations and species. In many cases, phenotypic variation in a hybrid population not only will be greater than that found in each parent population, but also will exceed the combined variation of both parent populations; this is known as transgressive segregation. The novel genetic diversity often will be maladaptive, resulting in hybrids that are inviable or have relatively low fitness. At times, however, the genetic reshuffling may result in stable populations with unique phenotypes, and when this happens a new species may emerge.

The extremely high levels of genetic diversity in populations of the outcrossing monkey flower Mimulus guttatus have been attributed to long-term introgression of genes from the selfing congeneric M. nasutus into M. guttatus (Sweigart and Willis, 2003). Another example of this phenomenon has been found in populations of Darwin's ground finches (genus Geospiza), which experience regular bottlenecks often caused by environmental extremes such as drought or excessive rainfall. Despite these bottlenecks, populations show little evidence of depleted genetic diversity, and this seems to be at least attributable partly to ongoing hyridization among all six species (Freeland and Boag, 1999). The generation of genetic diversity following hybridization has been cited as one reason for the rapid evolutionary change that has led to adaptive radiation after species invade new environments, two examples of this being Darwin's finches on the Galapagos archipelago and African cichlid fish in Lake Malawi (Seehausen, 2004). The acquisition of new genes through introgression can also be of practical concern because bacteria frequently exchange antibiotic resistance genes. In an unusual case, there is evidence that some of these bacterial genes have even crossed a kingdom boundary and been incorporated into a fungal genome (Penalva et al., 1990).

Inbreeding

Inbreeding occurs when individuals mate with their relatives. Inbreeding does not alter the allele frequencies within a population but it does increase the proportion of homozygotes at all loci, thereby decreasing levels of individual genetic diversity. Inbreeding therefore will reduce a population's diversity when measured as Ho, although it will not immediately affect He; however, as we will see in Chapters 6 and 7, inbreeding is a potential concern because it can reduce fitness levels, and if this happens it will deplete all measures of genetic diversity through increased mortality rates.

Historically, the only way to estimate inbreeding was from detailed pedigree records, a method that is completely impractical for most wild populations. Fortunately, the advent of molecular markers has provided alternative methods. Key to these methods is the identification of alleles that are identical by descent, i.e. alleles that are copies of a single allele that existed in a relatively recent ancestor. Individuals that have two alleles that are identical by descent are autozygous and must, by definition, be homozygous at the locus in question. This contrasts with allozygous individuals, which have two alleles that are not identical by descent (Figure 3.12). Note that allozygous individuals can be either homozygous or heterozygous at the locus in question because an allozygous individual may have

Figure 3.12 Diagram showing how both allozygous and autozygous individuals can be generated within the same family. Two unrelated heterozygotes in generation 1 produced four offspring, all with different parental alleles (generation 2). Inbreeding occurs among the siblings of generation 2, resulting in two allozygous and one autozygous individual in generation 3. Note that the allozygous individuals include both a heterozygote and a homozygote

Figure 3.12 Diagram showing how both allozygous and autozygous individuals can be generated within the same family. Two unrelated heterozygotes in generation 1 produced four offspring, all with different parental alleles (generation 2). Inbreeding occurs among the siblings of generation 2, resulting in two allozygous and one autozygous individual in generation 3. Note that the allozygous individuals include both a heterozygote and a homozygote two copies of the same allele that did not originate in a recent common ancestor. For this reason, estimates of inbreeding are not exactly the same as measures of observed homozygosity.

As noted earlier, the first clue that a population may be inbred is a deviation from Hardy--Weinberg equilibrium caused by Ho deficits. Observed and expected heterozygosity values form the basis of the inbreeding coefficient (F), which can be calculated as:

where HI is the frequency of heterozygous genotypes in a population at the time of investigation (individual heterozygosity) and HS is the frequency of heterozygotes that would be expected if the population was in HWE (populations are commonly referred to as subpopulations in the literature surrounding the theory of F, hence subpopulation heterozygosity). In other words, F measures the reduction in heterozygosity compared with the heterozygosity that we would expect to find in a randomly mating population with the same allele frequencies. When F = 0 there is no inbreeding at all. At the other extreme, when F = 1, all individuals within a population are homozygous and there may be complete inbreeding. It is, however, worth reiterating that a deficit of heterozygotes is not always due to inbreeding because population substructure (Wahlund effect), null alleles or natural selection may also contribute. Table 3.9 provides some estimates of F in wild populations.

In vertebrates, which (with a few exceptions) are relatively invariant in their reproductive modes, inbreeding is more likely to occur in small, isolated

Table 3.9 Some examples showing the range of average population inbreeding coefficients (F) across a variety of taxonomic groups. The examples in this table also show how F varies within a species, depending on whether the population reproduces predominantly by sexual or asexual means, or whether F is calculated for adults or offspring

Inbreeding coefficient (F)

Species

Marker

Inbreeding coefficient (F)

within populations

Reference

Asexual: 0.339

Delmotte et al. (2002)

Sexual: 0.020

Asexual: -0.499

Sexual: 0.182

Asexual: 0.033

Simon et al. (1998)

Sexual: 0.244

Offspring: -0.068

Lawler, Richard and

Adults: 0.003

Riley (2003)

Native (continental):

Merila, Bjorklund and

0.133

Baker (1996)

Introduced (island):

0.124

Metal-tolerant: 0.217

Dubois et al. (2003)

and 0.501

Metal-intolerant: 0.578

and 0.704

Seeds: 0.163

Morand et al. (2002)

Adults trees: 0.292

Aphids (Rhopalosiphum Allozymes padi)

Microsatellites

Aphids (Sitobion avenae) Lemurs (Propithecus verreauxi) Greenfinch

(Carduelis chloris)

Microsatellites Microsatellites Allozymes

Alpine pennycress Allozymes

(Thlaspi caerulescens)

Common ash Microsatellites

(Fraxinus excelsior)

populations because of the increased likelihood of mating with a relative even when mating is random. In other taxa that have two or more methods of reproduction, such as many plants and invertebrates, inbreeding may be influenced further by a species' ecology. The succulent shrub Agave lechuguilla that grows in the Chihuahan Desert can undergo either clonal or sexual reproduction. Sex can involve either outcrossing, which occurs when pollinators transfer pollen between plants, or self-pollination (selfing), which is the most extreme form of inbreeding. The main pollinators of A. lechuguilla are nocturnal hawk moths (Hyles lineata) and diurnal large bees (Bombus pennsylvanicus and Xylocopa californica). A comparison of A. lechuguilla populations from different latitudes found that populations further north have fewer visits by pollinators compared with those in the southern part of its range (Silva-Montellano and Eguiarte, 2003a). They also had relatively low Ho values, although He values were comparable across latitudes. The authors of this study concluded that, in populations with fewer pollinators, self-pollination is more common and this results in inbreeding and therefore relatively high levels of Ho (Silva-Montellano and Eguiarte, 2003b; Figure 3.13).

Figure 3.13 Relationship between the number of visits by pollinators and the levels of inbreeding in Agave lechuguilla populations. Populations at higher latitudes are visited less frequently by pollinators than those further south. With fewer pollinators, selfing becomes more common and the observed heterozygosity (Ho) decreases. Data from Silva-Montellano and Eguiarte (2003a,b)

Figure 3.13 Relationship between the number of visits by pollinators and the levels of inbreeding in Agave lechuguilla populations. Populations at higher latitudes are visited less frequently by pollinators than those further south. With fewer pollinators, selfing becomes more common and the observed heterozygosity (Ho) decreases. Data from Silva-Montellano and Eguiarte (2003a,b)

Was this article helpful?

0 0

Post a comment