Table S1. Threatened/near threatened species and populations where gene flow has been augmented for conservation purposes to alleviate genetic problems
(known or suspected).
Common name Taxa References
Mammals
African elephant
African lion
African wild dog
Loxodonta africana
Felis leo
Lycaon pictus
Frankham (2009a)
Trinkel et al. (2008);
Frankham (2009a)
Davies-Mostert et al.
Black rhinoceros
Bighorn sheep
Diceros bicornis
Ovis canadensis
(2009)
Frankham (2009a)
Hogg et al. (2006)
Columbia Basin pygmy rabbit Brachylagus idahoensis Goodall et al. (2009)
Florida panther Puma concolor coryi Hedrick and Frederickson
Golden lion tamarin
Mexican wolf
(2010)
Leontopithecus rosalia Frankham et al. (2010)
Canis lupus baileyi Hedrick and Frederickson
Outbreeding depression – Page 1

(2010)
Cardoso et al. (2009) Northern quoll
Birds
Greater prairie chicken in Illinois
Red-cockaded woodpecker
Dasyurus hallucatus
Tymphanuchus cupido Westemeier et al. (1998) pinnatus
Piciodes borealis U.S. Fish and Wildlife
Service (2003)
Reptile
Swedish adder
Plants
Button wrinklewort
(within ploidy levels)
Lakeside daisy population in Illinois
Marsh grass of Parnassus
Vipera berus
Rutidosis leptorrhynchoides
Hymenoxys acaulis var. glabra
Parnassia palustris
Madsen et al. (2004)
Pickup and Young (2007)
Demauro (1993)
Bossuyt (2007)
Mauna Kea silversword Argyroxiphium sandwicense
Robichaux et al. (1997)
Brown’s banksia ssp. sandwicense )
Banksia brownii Barrett and Jackson
(2008)
Round leafed honeysuckle Lambertia orbifolia Coates et al. (1998)
Outbreeding depression – Page 2

All species with fragmented distributions and at least one isolated population (no gene flow) can eventually benefit genetically from augmented gene flow (Frankham et al.
2010). The smaller the effective population sizes the sooner populations need augmented gene flow. For sexual species the benefits are increased genetic diversity, reduced inbreeding and increased reproductive fitness, whilst asexual species benefit from augmented genetic diversity. Metapopulations are especially susceptible to extinction from inbreeding (Saccheri et al. 1998; Tallmon et al. 2004). Island populations typically have reduced genetic diversity and are inbred compared to mainland populations and would benefit from re-establishment of gene flow (Frankham 1997,
1998). Many of the species on the planet fall into the above categories, including many threatened species of animals and plants in the IUCN Red List, most of which have fragmented distributions (World Conservation Monitoring Centre 1992; IUCN 2010).
Frankham et al. (2010) alone listed the following taxa that fall into the category: blackfooted rock wallabies on islands and fragmented mainland populations in Australia, koalas on islands and the mainland in Victoria and South Australia, giant pandas in
China, black rhinoceros in Kenya, leopards in South Africa, ghost bats, Cunningham’s skink and matchstick banksias in Australia, Indian rhinoceroses, black-footed ferrets, grizzly bears, wolves, desert topminnow fish, and plants scarlet gilia, spreading avens and swamp pink in North America, tuataras on New Zealand offshore islands, Glanville fritillary butterflies in Finland, several species of birds in New Zealand, especially those
Outbreeding depression – Page 3

with several island populations, and several species in the Tumut fragmentation study in
Australia (in addition to the cases in Table 1).
Many mammal, bird, fish, lizard and plant species in Australia, Europe, North and South
America and Martinique show evidence of the merging of previously isolated and differentiated populations following climatic cycles (Soltis et al. 1997; Avise 2000; Hewitt
2000; Taylor et al. 2006; Antunes et al. 2008; Arnold et al. 2008; Grant & Grant 2008;
Schwenk et al. 2008; Hu et al. 2009; McDevitt et al. 2009; De Carvalho et al. 2010;
Thorpe et al. 2010). For example, several Australian rainforest vertebrate species have gone through cycles of isolation and rejoining (Joseph et al. 1995).
Many animal and plant species have become invasive following merging of genetically differentiated colonists (Ellstrand & Schierenbeck 2000; Kolbe et al. 2007).
For example, many populations of Australian brushtail possums in New Zealand represent “successful” merging of mainland Australia and Tasmania sub-species (Taylor et al. 2004).
There are many fewer published studies reporting outbreeding depression than inbreeding depression: the Web of Science from 1945-May 2010 revealed 379 references when “outbreeding depression” was a key word compared to 3,369 references for when “inbreeding depression” was used. However, this might reflect
Outbreeding depression – Page 4

different research efforts devoted to the two phenomena. In a sample of 13 species,
Edmands (2007) found that inbreeding depression was more frequent than F1 outbreeding depression, but that F2 outbreeding depression occurred with a similar frequency to inbreeding depression (based on data from only eight species). However, the largest data set on the issue, a fish meta-analysis involving 576 F1 and 94 F2 crosses by McClelland and Naish (2007), found that the average effect of crossing across all traits and all environments was significantly beneficial, indicating heterotic effects (the converse of inbreeding depression) are more common than outbreeding depression. Further, F1 and F2 effects were not significantly different.
The impacts on reproductive fitness of crossing population that differ by centric fusions may be small or undetectable. Introduction of house mice from the Orkney Island of
Eday into the genetically depauperate Isle of May population was successful in spite of the populations differing by three fixed centric fusions (Scriven 1992).
The deleterious effects of inversion polymorphisms arise because single (and other odd-numbered) crossovers result in unbalanced gametes (duplicated and deficient gene contents). The probability of a single crossover increases with the size of the inversion , and thus the deleterious effects increase correspondingly, as has been observed empirically (Coyne et al. 1993). As recombination rates vary along chromosomes, the increase in crossover rate with inversion size will not necessarily be proportional, but it will be an increasing probability function. This effect is not observed
Outbreeding depression – Page 5

for all inversions, presumably due to lack of chromosomal pairing and crossing over in the inverted region (Coyne et al. 1993), meaning that our predictions of risks due to fixed inversions differences between populations will sometimes be overly conservative.
The following references also conclude that genetic adaptation to different environments drives most cases of rapid development of reproductive isolation (Rice & Hostert 1993;
Schluter, 2001; Gavrilets 2004; Funk et al. 2006; Langerhans et al. 2007; Price 2008;
Rolshausen et al. 2009; Stelkens & Seehausen 2009; Sobel et al. 2010; Thorpe et al.
2010; Wang & Summers 2010).
Recent molecular evidence indicates that for large populations in the same environment the same loci and alleles are repeatedly involved in evolutionary change in large isolated replicates. For example, Hohenlohe et al. (2010) found rather similar patterns in
45,000 SNPS in parallel adaptations in three-spined sticklebacks and others have previously found that independent cases of benthic versus limnetic adaptations in this species repeatedly involve the same allele at the same locus (Colosimo et al. 2005).
Further, the melanocortin-1 receptor ( Mc1r ) is repeatedly (but not exclusively) involved in adaptation in external pigmentation across mammals, birds and reptiles (Hoekstra
Outbreeding depression – Page 6

2006). Further, the same insecticide resistant mutations are often observed across populations and species (McKenzie & Batterham 1994; Hartley et al. 2006). For dieldrinresistance, amino acid substitutions at the same site may be responsible for resistance in three insect orders. These studies indicate that the evolution of different coadapted gene complexes in replicate populations in the same environment is improbable unless there is a significant drift component. However, when drift is significant the populations will also become inbred, have reduced genetic diversity and have lowered adaptation and show genetic rescue effects upon crossing that would to a degree mask any outbreeding depression (OD) due to coadapted gene complexes. Different coadapted gene complexes are more likely to evolve in population in different, rather than similar environments as the selective forces are likely to be partially different and so favor different genetic variants (Pickup 2008).
Postzygotic reproductive isolation that is not a direct consequence of adaptation to different environments is widely viewed as arising primarily from Dobzhansky-Muller incompatibilities (Dobzhansky 1937; Muller 1940; see Coyne & Orr 2004; Presgraves
2010). However, these may often arise later in the speciation process (Muller 1940;
Presgraves 2010; but see Coyne & Orr 2004) beyond the 500 years we have defined for the occurrence of OD in recently fragmented populations. In brief, Dobzhansky-Muller incompatibilities involve a two (or more) loci system, with initial homozygous genotype aabb . Independent mutations in the A and B loci occur in two allopatric populations and
Outbreeding depression – Page 7

rise to fixation, yielding AAbb and aaBB genotypes in the respective populations.
Crossing of these genotypes is difficult or impossible, due to incompatibilities of the A and B alleles, resulting in reproductive isolation. Fixation of the new mutations may occur through mutation pressure, genetic drift or natural selection, with the former two typically being slower than for prezygotic isolation. The probability of natural selection being involved will be greater when the two populations are in different environments.
For example, Christie and McNair (1984) have described plant populations with complementary lethal factors, one being a copper tolerant allele that results in lethality in populations from non-polluted environments, but it confers normal viability in a copper tolerant population on copper polluted mine tailing. Cases involving natural selection are encompassed within our predictions (Predicting the Probability of Outbreeding
Depression).
The development of Dobzhansky-Muller incompatibilities involve the waiting time for the occurrence of mutant alleles where the mutation rate is approximately 10 -5 per locus per generation. Most such mutant alleles are lost by chance. The probability of eventual fixation of a new neutral mutation is its initial frequency 1/(2 N e
), whilst the probability is 2s N e
/ N if the mutant is favored by selection (where s is the additive selection coefficient favoring it in heterozygotes) (Kimura 1983). A neutral mutation whose frequency reaches fixation takes on average of 4 N e
generations to do so. A favored mutant allele with a selective advantage of 1%, has a probability of fixation of only 0.2%, given that N e
/ N is approximately 0.1 (Frankham 1995). On average 500 such mutations have to occur before one is fixed, so the process will be slow unless the population size is large. Times to develop Dobzhansky-Muller incompatibilities will be
Outbreeding depression – Page 8

shorter if they involve pre-existing genetic variants, but this was not what was envisaged by the initiators of the hypothesis.
One version of Dobzhansky-Muller incompatibilities that has been observed empirically involves silencing of alternative duplicated loci in different isolated populations (Lynch & Conery 2000). The rise to fixation of a non-functional (null) allele is expected to be a neutral or near-neutral process (Lynch & Conery 2000). For a duplicated gene pair, loss of function of one copy takes on average a few million years
(Lynch & Conery 2000), well beyond our time frame. Incompatibilities due to duplicated histidine locus silencing were found in Arabidopsis thaliana (Bikard et al. 2009). Coyne and Orr (2004) doubt this is a common scenario, but to date it is one of the only two known case of Dobzhansky-Muller incompatibilities identified between populations within species that have been studied at the molecular level (Presgraves 2010).
An alternative version of the duplicated gene situation involves functional divergence of the two loci, driven by selection. This has occurred in many circumstances, including for duplicated hemoglobin loci in vertebrates. For examples, hemoglobins often differentiate in response to different environments, such as altitude
(Storz 2007). In general, cases where natural selection drives development of incompatibilities are more probable when populations inhabit different environments than when they inhabit similar ones. Molecular analyses typically reveal that similar loci are involved in adaptations to similar environments and different ones in disparate environments (see Coadapted Gene Complexes and Genetic Drift above), as encompassed in our predictions (Predicting the Probability of Outbreeding Depression).
Outbreeding depression – Page 9

Based upon a review of molecular analyses on hybrid dysfunction loci,
Presgraves (2010) concluded that “the first steps in the evolution of hybrid dysfunction are not necessarily adaptive ”, but this conflicted with the view of Maheshwari et al.
(2008) who concluded that “most HI (hybrid inviability) genes identified to date show evidence of positive selection.
” The proposed evolutionary bases of changes described by Presgraves (2010) were duplicate gene silencing (as above), mutation pressure, host-pathogen genetic conflicts, and genetic conflicts. Of 14 loci, only three involved intraspecific effects, two involved duplicate gene silencing (see above) and one hostpathogen conflict and all were in Adabidopsis thaliana, a selfing species where drift effects are likely to be large (Probabilities of Inbreeding and Outbreeding Depression in species with Different Breeding Systems: Selfing Species below). Changes due to mutation pressure alone will be extremely slow and outside our time scale of relevance
(Frankham et al. 2010). Host-pathogen conflicts involve either different evolutionary paths of adaptation to the same pathogen, with initial divergence due to genetic drift followed by selection, or more likely adaptation to different pathogens which falls into the realm of different environments. Selfish genetic elements (transposons, meiotic drive elements and gamete killing segregation distorters) have evolutionary interests that conflict with those of their hosts. Hosts typically evolve means to suppress the deleterious impacts of selfish elements. Postzygotic OD from selfish elements will arise either from crossing populations with and without the selfish elements, or from incompatibilities from different host loci evolved to suppress the deleterious impacts of the elements (with initial divergence due to genetic drift). It is unclear how rapidly such differences will evolve in populations that have only recently been isolated. Those
Outbreeding depression – Page 10

requiring genetic drift to generate initial differences will typically be associated with genetic rescue effects that will tend to mask them (Frankham et al. 2010).
Overall, the evolution of OD via postzygotic isolation will often occur beyond our time frame, or involve differential adaptation to disparate environments.
Equations 1 and 2 have simplifying assumptions as detailed below, but have been experimentally validated and are widely used in quantitative genetics and animal breeding. The first assumption for equation 1 is that the drift term

(1 – 1/[2 N e
]) t
– 1 is not unduly affected by selection. This assumption was first made by Alan Robertson, on the basis that many loci are likely to be affecting quantitative traits so that selection per locus is weak, and is widely used in quantitative genetics and animal breeding
(Robertson 1960, 1970; James 1972; Bulmer 1980; Hill 1982a, b; Hill & Caballero
1992). The second assumption is that disequilibrium generated by selection (Bulmer
1980) has minor impacts. The drift term has been shown to be a very good approximation over 50 generations from experiments in invertebrates, mammals and plants (Weber 2004), and for populations subjected to short severe bottlenecks in population size and subsequently subjected to many generations of artificial selection
(see Frankham 1980). Similar assumptions are inherent in equation 2 (Hill 1982a, b) and again empirical tests have shown them to be adequate for the current purposes
(Hill 1982b; Frankham 1983).
Outbreeding depression – Page 11

The Sh 2 part of equation 1 has been supported in numerous empirical tests (Hill
& Caballero 1992; Falconer & Mackay 1996). S i
is used in equations 1 and 2 as the selection differential for reproductive fitness will decline with generations, as the adaptation to its new environment saturates (Gilligan & Frankham 2003). We assume that adaptation in the source population has saturated, such that its mean reproductive fitness is stable genetically. If there are environmental fluctuations, then the adaptive difference may fluctuate around the predicted difference if the average environment is not changing.
When two populations move to new environments a and b , their adaptive divergences from the source population will be as given by scenario 1, while their differentiation from each other will depend upon the difference between the two environments. Since the heritabilities, selection differentials, effective population sizes and generation lengths in the two environments may be different, the precise form of the equation for the adaptive differentiation between the two environments is: t ta ta

AD t
~ E { h a
2 
Sa i
(1
– 1/[2
N e a
]) t
– 1
+

2 N e a
Sa i
σ m a
2 /
σ
P a
2 + i = 1, i = 1, i = 1, tb tb
h b
2 
Sb i
(1
– 1/[2
N e b
]) t
– 1
+

2 N e b
Sb i
σ m b
2 /
σ
P b
2 } i = 1, i = 1,
(S1) where the terms are as defined for equations 1 and 2, except that a and b reflect their specific values in environments a and b . If the two environments differ in
“all” respects, then the adaptation will be the sum of that in populations a and b ( E = 1). However, if
Outbreeding depression – Page 12

the environments differ from that of the source population in characteristics x and y , and y and z , respectively, then the adaptive differentiation between them will reflect adaptation to x and z (with that to y being similar if they have similar effective sizes, reproductive rates and generation lengths). The degree of adaptive differentiation between populations has been shown in a meta-analysis to increase with the environmental difference between populations, as predicted (Hereford 2009).
For simplicity, the number of generations is measured from complete cessation of gene flow between the populations. If gene flow dribbles to a stop, there may be a small amount of adaptive differentiation before complete cessation.
High levels of non-additive genetic variation for fitness traits are usually attributable to a prior history of directional natural selection in a relatively stable environment (Mather
1973; Crnokrak & Roff 1995; Frankham 2009b). However, this does not apply to populations moved to new environments, where we expect them to exhibit ample amounts of predominantly additive genetic variation for fitness traits. As expected, de
Oliveira and Cordeiro (1980) reported adaptive differentiation in Drosophila willistoni to new low or high pH medium environments was primarily due to additive effects. Further, fitness in populations adapting to new environments showed drift effects as expected with additivity from equation 1. (Frankham et al. 1999, 2010 p.238; England et al. 2003)
Even if there is non-additive genetic variation within a particular environment, it is the additive genetic variation that determines selection response and is the basis of
Outbreeding depression – Page 13

predictions of response in animal and plant breeding, as used herein (Falconer &
Mackay 1996).
Our models predict that the development of reproductive isolation will be more closely related to generations than years, other things being equal. Marzluff and Dial (1991) found that speciose taxa of vertebrates, invertebrates and plants were all characterized by short generation times, compared to lower species diversity groups.
As genetic distances between species for neutral markers are an increasing function of generations, we expect a positive relationship between reproductive isolation and genetic distance (provided effective population sizes are of similar magnitudes).
Such relationships have been reported in Drosophila , copepods, Lepidoptera, frogs, birds and two of three plant genera investigated (Coyne & Orr 1997; Sasa et al. 1998;
Edmands 1999; Presgraves 2002; Price & Bouvier 2002; Moyle et al. 2004). Further,
Kisel and Barrowclough (2010) have shown that speciation rates are related to reduced gene flow and area (an indicator of population size) across a broad array of taxa.
Reductions in gene flow in large populations are expected to enhance adaptation to different environments (when the gene flow is from a closely related population), as it reduces the flow of maladapted alleles. Isolation is a cornerstone of allopatric speciation, widely recognized as the most common form of speciation (Mayr 1963;
Coyne & Orr 2004).
Outbreeding depression – Page 14

Our predictions apply to outbreeding diploid or amphidiploid (allopolyploids that behave as diploids), but require modification for species with other breeding systems, as described below.
Asexual Species
Asexual eukaryotic species and populations without genetic diversity have limited potential to show adaptive evolution, as they rely on recent mutations for genetic change. Further, they do not have sexual reproduction and inbreeding or outbreeding so neither inbreeding nor outbreeding depression will occur, unless there is some sexual reproduction. If there are several clones, each will have been subject to a founder effect, such that different coadapted gene complexes among clones are likely. In yeast,
500 generations of asexual divergence in disparate environments resulted in a 46% reduction in hybrid fitness, whilst hybrids of parallel adapted populations experienced a
28% reduction in fitness (Dettman et al. 2007).
For species with a mixture of asexual and sexual reproduction we expect selection to utilize a higher proportion of non-additive genetic variation than for exclusively sexually outbreeding species, and for them to show coadaptation of alleles within clones. As predicted, cyclically parthenogenetic Daphnia show reduced fitness as a result of crossing between clones within populations (Lynch & Deng 1994; Deng &
Outbreeding depression – Page 15

Lynch 1996). They are expected to show OD in crosses between populations, but if the populations are in similar environments, the magnitude may not be substantially higher than for crosses within populations. We are not aware of relevant data on this comparison.
Selfing Species
Strictly selfing species do not outcross and so OD will not occur. However, most selfing species have at least occasional outcrossing and they typically exhibit less inbreeding depression than outbreeding species (Byers & Waller 1999). Selfing results in population bottlenecks and greatly reduces the likelihood of gene flow, so selfing species are expected to have isolation that is stronger and adaptation that is greater over shorter distances, with consequent higher risk of coadapted gene complexes and
OD (Dudash & Fenster 2000). Conversely, selfing species have lower levels of genetic diversity on average than outbreeders and lower effective population sizes, and lowered rates of adaptation for these reason (Li 1976; Hamrick & Godt 1989; Charlesworth &
Charlesworth 1995). Hereford (2010) reported similar adaptation of selfing and outcrossing plants in a meta-analysis, indicating that the two effects are of similar magnitudes. With similar adaptation, greater isolation and less recombination, selfing species are probably more likely than outbreeders to develop OD (Dudash & Fenster
2000), but we are unaware of comparison of OD in selfing and outbreeding species.
Such information is sorely needed.
Outbreeding depression – Page 16

Polyploid Species
The same predictor variables will apply in both diploid and polyploid populations, but the rates of adaptive differentiation may differ (Dudash & Fenster 2000). For example, loss of neutral genetic diversity will be slower in tetraploids than diploids for the same N e
(Frankham et al. 2010). Non-additive effects may be more common in polyploids than diploid species, but there is little empirical evidence (Dudash & Fenster 2000).
Polyploids may be less susceptible to inbreeding depression than diploids (other things being similar), as homozygosity is achieved more slowly in polyploids (Frankham et al.
2010). Empirical evidence is equivocal, but trends generally in this direction (Ramsey &
Schemske 2002).
Haplodiploid Species
Haplodiploid species are less sensitive to inbreeding depression than equivalent diploid species, due to purging of deleterious alleles in haploid males (Peer & Taborsky 2005;
Frankham et al. 2010). For equivalent sized populations, haplodiploids are expected to retain less genetic diversity than diploids, and this has been observed empirically
(Frankham et al. 2010). Thus, rate of adaptation in haplodiploids is probably slower than in diploids, other things being equal. Consequently, the development of OD is expected to be slower in haplodiploids and the extent of genetic rescue effects less than in equivalent diploids. Outbreeding depression, but little or no inbreeding depression has been reported in haplodiploid ambrosia beetles ( Xylosandrus germanicus ) and fig
Outbreeding depression – Page 17

wasps ( Platyscapa awekei ) that practice substantial sib mating (Peer & Taborsky 2005;
Greeff et al. 2009).
Generations are reported as the average since the two populations separated from the common ancestral population (not as the sum of the generations from one population to the other through the common ancestor).
The use of the following data sets in Table S2 to estimate generations to develop
OD in similar environments depends upon them being isolated populations and having sufficient genetic diversity and large enough effective population sizes to evolve. In most cases these conditions are satisfied. In all cases except the anole lizards, the population crosses did not show OD. In the anole lizards there is considerable gene flow between the populations following the geological uplift that connected their island homes (but whether there is any OD is unclear).
Table S2. Generations without development of outbreeding depression in similar environments and characteristics of the populations used.
____________________________________________________________________
Species Isolation References Generations of isolation
Population sizes Adaptive
(parents/generation changes possible
Outbreeding depression – Page 18

____________ __________
Three-spined stickleback fish
( Gasterosteus
~ 6,000
_______
Yes spp)
Thousands of stocks from
Up to ~ 2,400 several species of Drosophila
Drosophila pseudoobscura
280
Yes
Yes
Cowpea weevil
( Callosobruchus maculatus
Caribou
( Rangifer tarandus
Brushtail
)
)
230-250
~ 750
~ 1,700
Yes
Yes
_______________
Variable often modest, possibly ≥
50
__________
Very large (Lakes) Yes (evolved benthic and
Lymnetic forms)
Likely
_________
Rundle et al.
(2000)
Coyne & Orr
(2004)
Several thousand Yes
High initial genetic diversity
400
(cross of 4 populations)
Probable
Several
Ehrman
(1969) hundred founders per population from the wild,
Bieri &
Kawecki
(2003)
Unknown, but probably relatively large
Probably > 1 Yes implying high genetic diversity
Yes McDevitt et al.
(2009)
Kerle et al
Outbreeding depression – Page 19

possums
( Trichosurus vulpecular )
Anole lizards
( Anolis roquet )
~ 6 million and Yes
~ 8 million million on mainland and ~ 100K in
Tasmania
Island populations, Yes for at presumably large least some populations, probable for the others
(1991); Taylor et al. (2004)
Thorpe et al.
(2010)
The Arabian oryx ( Oryx leucoryx ) population, which derives from population crosses, exhibits OD and is polymorphic for a translocation (Benirschke & Kumamoto 1991;
Marshall & Spalton 2000).
Extreme divergence in Copepods
The copepods studied by Edmands and colleagues exhibited an F
ST
of 0.80 for microsatellites and 0.98 for mtDNA (Edmands & Harrison 2003), with nuclear and mitochondrial patterns being “largely concordant” (Edmands 2001). Further, they have
“one of the highest levels of mitochondrial DNA differentiation ever reported among conspecific populations”, and interpopulation allozyme divergence is “about an order of magnitude higher than in most species”, “with one population exhibiting nearly complete reproductive isolation” (Edmands 2001). They could be an undescribed species
Outbreeding depression – Page 20

complex, as reported for another copepod “species” with similar divergences in mtDNA
(Lee 2000).
Apparent Outbreeding Depression in F2 Crosses between Sympatric Populations of Pink Salmon
In the pink salmon there were similar return rates (survival during the sea phase) of F1 hybrids between even- and odd-year populations and controls, but lower rates for F2 hybrids than controls. However, average size of hybrids exceeded that of controls in F1 and F2. Since size is related to fecundity in fish, this indicates effects of crossing on fitness in different directions for the F2 (i.e. increased fecundity may have offset decreased survival, so it is not known if there was any OD in total fitness) and benefits of crossing in the F1. These papers and others report strong reproductive isolation and relatively large genetic divergence for allozymes between the odd- and even-year forms
(reviewed by Allendorf & Waples 1995). There is also substantial structuring in mtDNA haplotypes that yields an estimate of 23,600 years since divergence between odd- and even-year forms (Churikov & Gharrett 2002). This may be an underestimate, as oddeven divergence may have evolved more than once. Glacial cycles have had a major impact on pink salmon and the two forms may have evolved in different refugia and only come into sympatry secondarily. The odd and even forms have partially different karyotypes, with even populations all having 52 chromosomes, while the odds also have high frequencies of individuals with 53 and 54 chromosomes (67% of these in the location nearest to the source of fish for the Gharrett studies) due to a polymorphic
Outbreeding depression – Page 21

centric fission. This confirms a high degree of reproductive isolation. The geographic distribution of even- and odd-forms are partially different (with substantial gene flow between populations within forms) (Churikov and Gharrett 2002), suggesting that they may be adapted to slightly different environments, perhaps differentiating in allopatry and only more recently coming into sympatry.
Our Guidelines May Preclude Gene Flow in More Cases than Strictly Necessary
Our guidelines would preclude gene flow between sub-species of orangutans ( Pongo pygmaeus ) (differ by a fixed inversion difference and isolated for 1.1-5 million years;
Warren et al. 2001; Zhang et al. 2001; Steiper 2006), domestic and Przewalski’s horses
( Equus caballus and E. przewalskii ; distinct species, differ by a fixed chromosomal difference and isolated for ~ 250,000 years; Monfort et al. 1991), and Asian and African lions ( Panthera leo ; isolated for ~ 100,000 years; Antunes et al. 2008). However, in all three cases no significant OD was found in captivity (Ballou 1995). Low statistical power is a possible reason for the lack of significant OD, or OD may not be exhibited in the artificial captive environments.
Our decision tree recommends against crossing of the Peromyscus beach and old-field sub-species on the basis of lack of gene flow in the last 500 years, but these crosses were beneficial (with heterosis effects being greater than OD). Our guidelines might recommend against augmented gene flow between the Florida panthers and
Texas cougars on the basis of habitat differences. This is a situation where substantial genetic rescue was expected and OD was also possible, the former due to the
Outbreeding depression – Page 22

population bottleneck in the panthers and the latter possible due to habitat differences.
The habitat differences between the two populations are relatively modest, compared to the very wide range of habitats exploited by the species. So far beneficial effects of outcrossing have been reported (Hedrick & Frederickson 2010). This could be due to either greater genetic rescue than OD effects, to there being no OD, or to OD not being exhibited until the F
2
or later (Fenster & Galloway 2000). There is currently insufficient data to evaluate these hypotheses.
Our use of gene flow within the last 500 years as the criterion for genetic isolation may be shorter than necessary (e.g. Peromyscus data). However, we prefer to take a conservative approach initially and await further data before altering it.
In spite of the above indications, our probability assessments will lead to many more genetic rescues than current practice or actions following the recommendations of
Edmands (2007).
Our work is related to the concepts of evolutionarily significant units, and exchangeability developed by Ryder (1986), Woodruff (1989), Fenster & Dudash
(1994), Waples (1995), Moritz (1999), Crandall et al. (20000 and Fraser & Bernatchez
(2001). However, the purpose of those concepts is primarily to define units within species that require separate management, whilst our focus is exclusively on OD, and especially on identifying populations where gene flow can potentially lead to genetic rescue and thereby minimize the probability of population extinction. All authors deal
Outbreeding depression – Page 23

with isolation, adaptive difference are considered by all except Moritz (1999), a time dimension is only explicitly considered by us and Crandall et al. (2000), and our proposal includes fixed chromosomal differences whilst only Ryder (1986) and Woodruff
(1989) mention chromosomes.
Allendorf, F. W., and R. S. Waples. 1996. Conservation and genetics of salmonid fishes.
Pages 238-280 in J. C. Avise, and J. L. Hamrick, editors. Conservation genetics: case histories from nature. Chapman & Hall, New York.
Antunes, A., et al. 2008. The evolutionary dynamics of the lion Panthera leo revealed by host and viral population genomics. PLOS Genetics 4 :e1000251.
Arnold, M. L., Y. Sapir, and N. H. Martin. 2008. Genetic exchange and the origin of adaptations: prokaryotes to primates. Philosophical Transactions of the Royal
Society of London Series B 363 :2813-2820.
Avise, J. C. 2000. Phylogeography: The history and formation of species. Harvard
University Press, Cambridge, Massachusetts.
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