
==== Front
Poult Sci
Poult Sci
Poultry Science
0032-5791
1525-3171
Elsevier

S0032-5791(24)00670-9
10.1016/j.psj.2024.104091
104091
GENETICS AND MOLECULAR BIOLOGY
Research Note: Study on the in-situ preservation of pigeons based on the level of endangerment of genetic resources
Li Xin *†
Hou Haobin *†
Shen Xiaohui *
Zhao Weimin ‡
Chen Yansen §
Yao Junfeng yaobison@163.com
*†1
Yang Changsuo *†
⁎ Shanghai Academy of Agricultural Sciences, Shanghai 201106, China
† National Poultry Engineering Technology Research Center, Shanghai 201106, China
‡ Shanghai Golden Royal Pigeon Industry Co. LTD, Shanghai 201508, China
§ Shanghai Pigeon Industrial Co. LTD, Shanghai 202152, China
1 Corresponding author: yaobison@163.com
11 7 2024
10 2024
11 7 2024
103 10 10409116 2 2024
7 7 2024
© 2024 The Authors
2024
https://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
The large-scale and intensive development of the meat pigeon breeding industry have resulted in the replacement of a large number of low-performance local breeds by a few breeds with excellent production performance. However, due to the characteristics of pigeon species that are monogamous, for which the W chromosome cannot be recovered and for which semen cannot be cryopreserved, the preservation of pigeon species is still mainly based on in-situ preservation. In this study, pigeons were classified into 6 classes of endangerment based on the criteria of the 100-year inbreeding coefficient of poultry populations in the “Assessment of Endangered Poultry Genetic Resources” (NY/T 2996–2016). The results show that when the generation interval was 1.5 yr, the number of ideal populations with the same gene frequency variance or the same heterozygosity decay rate of pigeons in class 1 to 5 was ≤149, 150 to 204, 205 to 316, 317 to 649 and ≥650. In random-reserved breeding, when the generation interval was 1.5 yr, the number of male (female) pigeons corresponding to class 1 to 5 was ≤74, 75 to 102, 103 to 157, 158 to 324 and ≥325. In family-equal-reserved breeding, when the generation interval was 1.5 yr, the number of male (female) pigeons corresponding to class 1 to 5 was ≤36, 37 to 50, 51 to 78, 79 to 162 and ≥163. When the generation interval was 1.5 yr, the inbreeding increments corresponding to class 1 to 5 were ≥0.00335, 0.00244 to 0.00334, 0.00159 to 0.00243, 0.00078 to 0.00158 and ≤0.00077; with the same population size, the inbreeding coefficient and inbreeding increment decreased with the increase of generation interval; the population effective content, inbreeding coefficient and inbreeding increment of family-equal-reserved pigeons were lower than those of random-reserved pigeons. The results of this study have certain reference value for analyzing the status quo of local and endangered species, constructing live gene banks and breeding farms of poultry genetic resources, and rescuing endangered species.

Key words

pigeon
living species preservation
effective population content
endangered rating
==== Body
pmcINTRODUCTION

Pigeons (Columba livia) are spectacularly diverse and exhibit variation in more traits than any other bird species (Murray et al., 2017). Other birds were bred for meat and egg production, but pigeons are thought to have been kept to aid agriculture. Their ability to fly long distances, select the richest nutrients, and then return to the same nesting place made their droppings an easily collectible source of rich fertilizer for growing crops in arid climates and on infertile land. As time went on, humans found more uses for pigeons. They are widely distributed worldwide and have been domesticated for thousands of years for the production of meat, for racing, for posting, or for ornamental purposes. They can be used as models to understand the molecular diversity of birds and other vertebrates, while classical breeding strategies and genomics can be used to analyze the different components of complex phenotypes and define the interactions between genes (Shapiro et al., 2013; Wang et al., 2020).

This genetic diversity may allow native varieties to be integrated into commercial breeding programs to develop new traits, such as diverse flavor and quality, disease resistance, and climate-specific traits in response to changing needs (Sun et al., 2022; Soule et al., 1980). However, under intensive genetic selection and pyramidal hybridization, a limited number of pure lines have been used for hybridization in commercial generations, while breeding for genetic uniformity and high-yield individuals have further shrunk the gene pool and weakened allelic polymorphisms (Joanne and Ellstrand, 2016; Zhang et al., 2019). Half of pigeon genetic diversity has been reduced due to generation selection and inbreeding for desirable traits in commercial breeding (Muir et al., 2008). Over the past 3 decades, a considerable proportion of avian genetic stocks has disappeared (Fulton and Delany, 2003), and many local varieties or groups with poor production performance and certain characteristics are on the verge of extinction. This not only represents a loss of existing resources, but also of pigeon-breeding material, with unpredictable consequences for future pigeon breeding.

Current cryopreservation methods apply only to sperm. The disadvantage of using semen for avian breed reconstruction is that it is not possible to recover the W chromosome and variation from the recipient population is incorporated in mitochondrial DNA (Silversides et al., 2012). In contrast to the livestock industry, sperm cryopreservation has not yet been successfully established in the poultry industry. The small head of pigeon sperm makes it difficult for cryoprotectant to enter the head, and the acrosome easily falls off during cryoresuscitation. And the tail is very long, which causes the sperm to break during various cryopreservation processes, reducing sperm motility (Janosikova et al., 2023). In addition, due to the characteristics of yolk in poultry germ cells, the cryopreservation technology of egg cells is limited in the protection of seed resources (Nakamura, 2017), and its mother egg cells (i.e., embryos) cannot be used for genetic resource preservation. Because there are currently no appropriate methods of cryopreservation available to the poultry industry, the long-term preservation of commercial elite stocks must continue to rely on live bird conservation (Fulton, 2006). For these reasons, in-situ breeding is currently the main practice of pigeon genetic resource conservation, which protects the original status, characteristics, and genetic diversity of pigeons to the greatest extent. In-situ conservation preserves the balance of a population gene pool (gene pool or gene bank) best, striving to ensure that every gene in it is preserved.

Genetic diversity conservation aims to protect existing pigeon genetic resources fully and appropriately, to prevent them from mixing and extinction; the main goal is to preserve the existing pigeon genetic resources in the gene bank as comprehensively as possible, regardless of whether these genes are currently valuable. Live bird conservation can dynamically conserve resources, but the set-up of a special pigeon breeding group is generally required, which is expensive to maintain, and can incur harmful management problems, such as inbreeding, the occurrence of harmful genes, and changes in population genetic structure caused by natural selection. The most widely recognized genetic reason for extinction risk is inbreeding depression, and there are many examples of high inbreeding depression in bird species, such as great tits, passenger pigeons, and house sparrows (O'Gradya et al., 2006; Fox et al., 2008). Even in the absence of systematic factors affecting the genetic structure of the live bird population, gamete-sampling errors can lead to random genetic drift of population gene frequencies, thus reducing conservation effort. An understanding of the most appropriate pigeon-breeding strategies is critical to avoid population genetic drift whilst minimizing breeding costs to preserve pigeon breeds. In this study, we used genetic, evolutionary, and ecological factors that influence the extinction and persistence of species in order to develop a conservation strategy. Research has shown that predictable systematic factors such as selection, mutation, migration, and mating patterns, as well as random, uncontrollable nonsystematic factors such as genetic drift, may cause the frequencies of genes and genotypes to fluctuate randomly, eventually affecting the genetic diversity of pigeon groups (Zhang et al., 2020; Mirrahimi and Gandon, 2020; Gibert, 2022) (Figure 1A–E). At the same time, with the increase of population generation, the number of pigeons with multiple alleles decreased gradually (Figure 1F).Figure 1 Changes in gene and genotype frequencies between pigeon generations (see attachment). (A) Changes in allele A frequencies at different initial gene frequencies when Ne is 80. During the gamete-sampling process, when the initial gene frequency was too high (0.9) or too low (0.1), the risk of a gene being fixed or lost due to random genetic drift was higher, which is not conducive to gene preservation. (B) The frequency change of allele A in different populations with the same initial gene frequency. At the same initial gene frequency, the larger the number of effective populations, the less likely alleles are lost.When the initial gene frequency was moderate, the risk of loss or fixation due to random genetic drift was lower. When the gene frequency was constant, the smaller the population (e.g., Ne = 10), the greater the gene frequency fluctuation. C, Frequency changes of genotype AA under different initial gene frequencies. The frequency variation of genotype AA was approximately similar to that of allele A. When the initial gene frequency was high (P = 0.9), the frequency of genotype AA still fluctuated at a relatively high level, gradually tended to 1, and became 1.0 in the 13th generation. When the initial gene frequency was low (P = 0.1–0.2), the gene frequency fluctuated at a low level and quickly approached 0. D, Frequency changes of genotype Aa under different initial gene frequencies. The frequency of genotype Aa was similar to the initial high (P = 0.8–0.9) and low (P = 0.1–0.2) levels. In both cases, the frequency of genotype Aa fluctuated at a low level and gradually tended to 0. E, Variation of aa frequency under different initial gene frequencies. The frequency fluctuation of genotype aa was opposite to that of genotype AA, showing that when the initial gene frequency was high, the frequency of genotype aa quickly tended to 0. F, Variations of number of polymorphic loci under different effective population sizes over generations.

Figure 1

Genetic resources are the foundation of new variety breeding and offer indispensable resources for human survival. In order to protect and rationally utilize pigeon genetic resources, it is necessary to scientifically assess the endangered species. According to the characteristics of diversity of pigeon genetic resources, we graded, assessed, and classified the endangerment of these resources and the population number range of each grade of endangerment was calculated. The results can be used in pigeon breeding in specific socio-economic and technical backgrounds.

MATERIALS AND METHODS

Basic Principles of Computer Software Simulation

The data of gene frequency and genotype frequency in this experiment are computer simulation data. Genetic drift refers to the phenomenon of random fluctuation of gene frequencies in small populations caused by random sampling errors, and is common in natural and domesticated conditions. For a group of pigeons with a population size of N and a pair of alleles a and A at a gene locus on an autochromosome. In the initial generation (generation 0), the frequency of A in the population is p, and the frequency of a is q = 1 − p. When 1 generation is produced, the population will generate a large number of gametes, from which 2N gametes are randomly selected to form N pigeons of 1 generation. Because each gamete carries only one of the genes (A or a), the frequency of generation 1 A is guaranteed to remain p and the frequency of generation 1 a is guaranteed to remain q only if there are 2Np A gametes and 2Nq a gametes among the 2N gametes that form generation 1. The same is true when generation 1 produces gametes to form generation 2. In reality, the limited size of the pigeon population means that sampling cannot be completely random, so the A gametes drawn are not necessarily 2Np, but fluctuate randomly around this value.

In the 2N gametes from generation 0 to generation 1, the number of times that gene A was drawn (x) conformed to the binomial distribution. All possible values of x are 0, 1, 2..., 2N, and its corresponding probability distribution function is P(x)=C2Nxp0xq02N−x (where p0 refers to the frequency of gene A in generation 0, and q0 refers to the frequency of gene a in generation 0). However, in a finite population, all possible values of x are random. Excel software was used to generate a random number between 0 and 1, which was equal to the cumulative probability of gamete A being extracted as ∑x=0ip(x). From this, we find a random value of i, and i2Nis the frequency p1 of gene A in generation 1.

When generation 1 forms generation 2, the corresponding probability distribution function of all possible values of x of the number of times that gene A is drawn: P(x)=C2Nxp1xq12N−x (where p1 refers to the frequency of gene A in generation 1, and q1 refers to the frequency of gene a in generation 1). Excel then generates another random number, which is also specified to be equal to the cumulative probability of gamete A being extracted: ∑x=0ip(x). Find the value of i, and the frequency of gene A in generation 2 (p2) is equal to i/2N. By analogy, we can calculate the values of p3, p4, p5 etc. Because q = 1 − p, the frequency of gene a changes accordingly. Once the frequency of gene A reaches 1 or 0, it becomes fixed or disappears, and “genetic drift” of the site stops.

In addition, we assume that 30 marker sites are selected according to microsatellite marker characteristics in the absence of genetic mutation. It is assumed that the loci are all located on different chromosomes, each loci has rich polymorphism, there are 4 ∼ 10 alleles, and there is no linkage and recombination interaction between each loci. After the Visual Studio 2019 Community Version software is installed, the program is written in Fortran90 language for prediction polymorphic bit number.

Polymorphic

A locus is considered polymorphic when the frequency of the most common allele is no greater than 0.95 (Ayala et al., 1972).

Classification of Endangerment

According to the 100-year inbreeding coefficient (F100), poultry populations are classified into 6 grades. The respective F100 values are as follows: (1) on the verge of extinction, F100 > 0.2; (2) seriously endangered, 0.15 < F100 ≤ 0.2; (3) endangered, 0.1 < F100 ≤ 0.15; (4) low risk of extinction, 0.05 < F100 ≤ 0.1; and (5) safe, F100 ≤ 0.05. Grade 6 indicates extinction, the presence of only single sex reproducible individuals or the absence of purebred individuals (NY/T 2996-2016).

Effective Population Size

The effective population size (Ne) is the number of breeding individuals that could give rise to sampling variance or the rate of inbreeding in the case of an idealized population. We use Ne to represent the ideal population size that can have the same gene frequency variance or the same heterozygosity decay rate as the actual population. We assume that the ideal population includes an adequate number of individuals and equal numbers of male and female individuals, with random mating, each individual producing the same number of offspring, no generation overlap, and no selection, mutation, migration, or other factors affecting the population genetic balance. Population size is the most important factor affecting the increase in average inbreeding coefficient. Genetic drift is more severe in small populations than in larger ones. For the ideal population size, the relationship is as follows (Falconer and Mackay, 1960):populationsize=Ne=12ΔF,

where △F represents the average inbreeding increment of the population.

Ideal Population Size

The ideal population is assumed to contain N diploid hermaphrodites, and when the population content is kept constant, the 2N independent gametes produced by these N individuals randomly combine into the next N individuals. Let a pair of alleles and their starting frequencies in the population be p and 1−p, respectively. If no other factors are taken into account, the sampling variance and heterozygous decay rates of parent–child gene frequencies in an ideal population of N individuals can be derived from the binomial distribution as p(1−p)2N and 12N, respectively.

Breeder Selection Manners

Random-Reserved Selection

Random-reserved selection means that the offspring of all male animals in the group is gathered to form the next generation of the population in a random mating way. It also means that some families may have more, fewer, or no offspring, regardless of the individual family distribution.

The formula for calculating the effective population size of the random-reserved population isNe=4Nm×NfNm+Nf=2Nm,

where Nm represents the number of male and Nf represents the number of female pigeons participating in breeding. Because pigeons have a 1:1 sex ratio, Nm is equal to Nf. The same holds below.

Family-Equal-Reserved

Family-equal-reserved selection is in accordance with the principle of the same number of offspring of the male family. In each generation, the number of lines selected is equal, and according to a 1:1 ratio of males and females to form the next generation, the next generation of male and female pairs must be produced from the previous generation of different male and female mates by random mating.

The formula for calculating the effective population size of the family-equal-reserved population isNe=16Nm×Nf3Nm+Nf=4Nm

Average Inbreeding Increment of Population

The value △F reflects the average homozygous rate of genes in the population genetic structure. When F0 of the initial population is zero, the relation between Ft and △F is as follows:Ft=1−(1−ΔF)t

In pigeon conservation population, ΔF is affected by population size, sex ratio (1:1), breeder selection manner and generation interval.

When the pigeons were kept at random-reserved selection, ΔF wasΔF=18Nm+18Nf=14Nm

When the pigeons were kept in family-equal-reserved selection, ΔF wasΔF=332Nm+132Nf=18Nm

Inbreeding Coefficient

The inbreeding coefficient is the probability that 2 alleles at a locus in an individual are identical by descent (Wright, 1922). The formula for the inbreeding coefficient isFt=1−(1−12Ne)t,

where Ne is the effective population size and t is the number of generations.

Generation Interval

The generation interval is the mean age of the parents at the time of birth of their progeny.

Pigeons reach sexual maturity at 6 to 7 mo of age, and we set generation intervals of 0.7, 1.0, 1.5, 2.0, 2.5, 3.0, 3.5, 4.0, 4.5, 5.0, 5.5, 6.0, 6.5, 7.0, 7.5, 8.0, 8.5, 9.0, 9.5, and 10.0 yr. In actual production, 1.5 yr is often used as the generation interval for pigeons.

RESULTS

Relationship Between Ne and Generation Interval in Pigeon Groups

As the generation interval increased, Ne of the 5 endangered classes gradually decreased (Table 1). When the generation interval was 0.7 yr, Ne of the populations categorized as on the verge of extinction, seriously endangered, endangered, low risk, and safe were ≤319, 320 to 439, 440 to 677, 678 to 1,392, and ≥1393, respectively. When the generation interval was 1.5, the Ne values were ≤149, 150 to 204, 205 to 316, 317 to 649 and ≥650, respectively. When the generation interval was 10.0, the respective Ne decreased to ≤22, 23 to 30, 31 to 47, 48 to 97, and ≥98, respectively. In the class of endangerment “safe” Ne respectively was greater than or equal to 1,393, 975, 650, 488, 390, 325, 279, 244, 217, 195, 177, 163, 150, 140, 130, 122, 115, 109, 103, and 98. At the same time, the decreases in Ne of the 5 grades gradually moderated with extension of the generation interval. As the interval between generations increased, the Ne of the 5 endangered classes gradually decreased.Table 1 Ne of 5 endangered classes for different generation intervals.

Table 1Generation interval (Year)	Class of endangerment	
On the verge of extinction	Seriously endangered	Endangered	Low risk	Safe	
0.7	≤319	320–439	440–677	678–1392	≥1393	
1.0	≤223	224–307	308–474	475–974	≥975	
1.5	≤149	150–204	205–316	317–649	≥650	
2.0	≤111	112–153	154–237	238–187	≥488	
2.5	≤89	90–122	123–189	190–389	≥390	
3.0	≤74	75–102	103–157	158–324	≥325	
3.5	≤63	64–87	88–135	136–278	≥279	
4.0	≤55	56–76	77–118	119–243	≥244	
4.5	≤49	50–68	69–105	106–216	≥217	
5.0	≤44	45–61	62–94	95–194	≥195	
5.5	≤40	41–55	56–86	87–176	≥177	
6.0	≤37	38–51	52–78	79–162	≥163	
6.5	≤34	35–47	48–72	73–149	≥150	
7.0	≤31	32–43	44–67	68–139	≥140	
7.5	≤29	30–40	41–63	64–129	≥130	
8.0	≤27	28–38	39–59	60–121	≥122	
8.5	≤26	27–35	36–55	56–114	≥115	
9.0	≤24	25–33	34–52	53–108	≥109	
9.5	≤23	24–32	33–49	50–102	≥103	
10.0	≤22	23–30	31–47	48–97	≥98	

Numbers of Male (Female) Pigeons in Each Endangered Class Under Random-Reserved Selection

The numbers of male (female) pigeons in the 5 endangered levels decreased as the number of generation intervals increased (Table 2). When the generation interval was 0.7 yr, the number of male (female) pigeons in the verge of extinction, seriously endangered, endangered, low risk, and safe categories were ≤159, 160 to 219, 220 to 338, 339 to 695, and ≥696, respectively. When the generation interval was 1.5 yr, the numbers of male (female) pigeons on the verge of extinction, seriously endangered, endangered, low risk and safe categories were ≤74, 75 to 102, 103 to 157, 158 to 324 and ≥325, respectively. When the generation interval was 10.0 yr, the numbers decreased to ≤10, 11 to 15, 16 to 23, 24 to 48, and ≥49, respectively. In the class of endangerment “safe” the number of male (female) pigeons respectively was greater than or equal to 696, 488, 325, 488, 244, 195, 163, 139, 122, 108, 98, 89, 81, 75, 70, 65, 61, 57, 54, 51, and 49. At the same time, the decreasing trend in numbers of male (female) pigeons in the 5 grades gradually tended to moderate with extension of the generation interval.Table 2 Numbers of male (female) pigeons in 5 endangered classes at random-reserved selection.

Table 2Generation interval (Year)	Class of endangerment	
On the verge of extinction	Seriously endangered	Endangered	Low risk	Safe	
0.7	≤159	160–219	220–338	339–695	≥696	
1.0	≤111	112–153	154–236	237–487	≥488	
1.5	≤74	75–102	103–157	158–324	≥325	
2.0	≤55	56–76	77–118	119–243	≥244	
2.5	≤44	45–61	62–94	95–194	≥195	
3.0	≤36	37–50	51–78	79–162	≥163	
3.5	≤31	32–43	44–67	68–138	≥139	
4.0	≤27	28–38	39–58	59–121	≥122	
4.5	≤24	25–33	34–52	53–107	≥108	
5.0	≤22	23–30	31–47	48–97	≥98	
5.5	≤19	20–27	28–42	43–88	≥89	
6.0	≤18	19–25	26–39	40–80	≥81	
6.5	≤16	17–23	24–36	37–74	≥75	
7.0	≤15	16–21	22–33	34–69	≥70	
7.5	≤14	15–20	21–31	32–64	≥65	
8.0	≤13	14–18	19–29	30–60	≥61	
8.5	≤12	13–17	18–27	28–56	≥57	
9.0	≤12	13–16	17–25	26–53	≥54	
9.5	≤11	12–15	16–24	25–50	≥51	
10.0	≤10	11–15	16–23	24–48	≥49	

Numbers of Male (Female) Pigeons in Different Endangered Classes Under Family-Equal-Reserved Selection

The numbers of male (female) pigeons in the 5 endangered classes gradually decreased with an increase in the number of generation intervals (Table 3). When the generation interval was 0.7 yr, the numbers in the verge of extinction, seriously endangered, endangered, low risk, and safe grades were ≤79, 80 to 109, 110 to 169, 170 to 347, and ≥348, respectively. When the generation interval was 1.5 yr, the numbers in the classes of verge of extinction, seriously endangered, endangered, low risk, and safe were ≤36, 37 to 50, 51 to 78, 79 to 162 and ≥163, respectively. When the generation interval was 10.0, the respective numbers decreased to ≤5, 6 to 7, 8 to 11, 12 to 23, and ≥24, respectively. In the class of endangerment “safe” the number of male (female) pigeons respectively was greater than or equal to 348, 244, 163, 122, 98, 81, 70, 61, 54, 49, 44, 41, 38, 35, 33, 31, 29, 27, 26, and 24. It can be seen that the number of species left for each endangered class is half of the number left for random-reserved selection. At the same time, the decreasing trend in numbers in the 5 grades gradually tended to moderate with extension of the generation interval.Table 3 Numbers of male (female) pigeons in 5 endangered classes under family-equal-reserved selection.

Table 3Generation interval (Year)	Endangered rating	
On the verge of extinction	Seriously endangered	Endangered	Lower risk	Safe	
0.7	≤79	80–109	110–169	170–347	≥348	
1.0	≤55	56–76	77–118	119–243	≥244	
1.5	≤36	37–50	51–78	79–162	≥163	
2.0	≤27	28–38	39–58	59–121	≥122	
2.5	≤21	22–30	31–47	48–97	≥98	
3.0	≤18	19–25	26–39	40–80	≥81	
3.5	≤15	16–21	22–33	34–69	≥70	
4.0	≤13	14–18	19–29	30–60	≥61	
4.5	≤12	13–16	17–25	26–53	≥54	
5.0	≤10	11–14	15–23	24–48	≥49	
5.5	≤9	10–13	14–21	22–43	≥44	
6.0	≤8	9–12	13–19	20–40	≥41	
6.5	≤8	9–11	12–17	18–37	≥38	
7.0	≤7	8–10	11–16	17–34	≥35	
7.5	≤7	8–9	10–15	16–32	≥33	
8.0	≤6	7–9	10–14	15–30	≥31	
8.5	≤6	7–8	9–13	14–28	≥29	
9.0	≤5	6–8	9–12	13–26	≥27	
9.5	≤5	6–7	8–12	13–25	≥26	
10.0	≤5	6–7	8–11	12–23	≥24	

Inbreeding Increment for Each Endangered Class Under Different Generation Intervals

The inbreeding increments in the 5 endangered classes gradually increased as the number of generation intervals increased (Table 4). When the generation interval was 0.7 yr, the inbreeding increments in the verge of extinction, seriously endangered, endangered, low risk, and safe classes were ≥1.570 × 10−3, 1.150 × 10−3 to 1.560 × 10−3, 7.500 × 10−4 to 1.140 × 10−3, 3.700 × 10−4 to 7.400 × 10−4, and ≤3.600 × 10−4, respectively. When the generation interval was 1.5 yr, the inbreeding increments in the classes of verge of extinction, seriously endangered, endangered, low risk, and safe were ≥3.350 × 10−3, 2.440 × 10−3 to 3.340 × 10−3, 1.590 × 10−3 to 2.430 × 10−3, 7.800 × 10−4 to 1.580 × 10−3, and ≤7.700× 10−4, respectively. When the generation interval was 10.0, the respective inbreeding increments decreased to ≥2.208 × 10−2, 1.613 × 10−2 to 2.207 × 10−2, 1.049 × 10−2 to 1.612 × 10−2, 5.130 × 10−3 to 1.048 × 10−2, and ≤5.120 × 10−3, respectively.Table 4 Inbreeding increments in 5 endangered classes for different generation intervals.

Table 4Generation interval (Year)	Class of endangerment	
On the verge of extinction	Seriously endangered	Endangered	Low risk	Safe	
0.7	≥1.570 × 10−3	1.150 × 10−3–1.560 × 10−3	7.500 × 10−4–1.140 × 10−3	3.700 × 10−4–7.400 × 10−4	≤3.600 × 10−4	
1.0	≥2.240 × 10−3	1.630 × 10−3–2.230 × 10−3	1.060 × 10−3–1.620 × 10−3	5.200 × 10−4–1.050 × 10−3	≤5.100 × 10−4	
1.5	≥3.350 × 10−3	2.440 × 10−3–3.340 × 10−3	1.590 × 10−3–2.430 × 10−3	7.800 × 10−4–1.580 × 10−3	≤7.700 × 10−4	
2.0	≥4.460 × 10−3	3.260 × 10−3–4.450 × 10−3	2.110 × 10−3–3.250 × 10−3	1.040 × 10−3–2.100 × 10−3	≤1.030 × 10−3	
2.5	≥5.570 × 10−3	4.060 × 10−3–5.560 × 10−3	2.640 × 10−3–4.050 × 10−3	1.290 × 10−3–2.630 × 10−3	≤1.280 × 10−3	
3.0	≥6.680 × 10−3	4.870 × 10−3–6.670 × 10−3	3.170 × 10−3–4.860 × 10−3	1.550 × 10−3–3.160 × 10−3	≤1.540 × 10−3	
3.5	≥7.790 × 10−3	5.680 × 10−3–7.780 × 10−3	3.690 × 10−3–5.670 × 10−3	1.800 × 10−3–3.680 × 10−3	≤1.790 × 10−3	
4.0	≥8.900 × 10−3	6.490 × 10−3–8.890 × 10−3	4.220 × 10−3–6.480 × 10−3	2.060 × 10−3–4.210 × 10−3	≤2.050 × 10−3	
4.5	≥1.000 × 10−2	7.300 × 10−3–9.990 × 10−3	4.740 × 10−3–7.290 × 10−3	2.320 × 10−3–4.730 × 10−3	≤2.310 × 10−3	
5.0	≥1.111 × 10−2	8.100 × 10−3–1.110 × 10−2	5.260 × 10−3–8.090 × 10−3	2.570 × 10−3–5.250 × 10−3	≤2.560	
5.5	≥1.221 × 10−2	8.910 × 10−3–1.220 × 10−2	5.790 × 10−3–8.900 × 10−3	2.830 × 10−3–5.780 × 10−3	≤2.820 × 10−3	
6.0	≥1.331 × 10−2	9.710 × 10−3–1.330 × 10−2	6.310 × 10−3–9.700 × 10−3	3.080 × 10−3–6.300 × 10−3	≤3.070 × 10−3	
6.5	≥1.441 × 10−2	1.052 × 10−3–1.440 × 10−2	6.840 × 10−3–1.051 × 10−2	3.340 × 10−3–6.830 × 10−3	≤3.330 × 10−3	
7.0	≥1.551 × 10−2	1.132 × 10−2–1.550 × 10−2	7.360 × 10−3–1.131 × 10−2	3.590 × 10−3–7.350 × 10−3	≤3.580 × 10−3	
7.5	≥1.661 × 10−2	1.212 × 10−2–1.660 × 10−2	7.880 × 10−3–1.211 × 10−2	3.850 × 10−3–7.870 × 10−3	≤3.840 × 10−3	
8.0	≥1.770 × 10−2	1.293 × 10−2–1.769 × 10−2	8.400 × 10−3–1.292 × 10−2	4.110 × 10−3–8.390 × 10−3	≤4.100 × 10−3	
8.5	≥1.880 × 10−2	1.373 × 10−2–1.879 × 10−2	8.930 × 10−3–1.372 × 10−2	4.360 × 10−3–8.920 × 10−3	≤4.350 × 10−3	
9.0	≥1.989 × 10−2	1.453 × 10−2–1.988 × 10−2	9.450 × 10−3–1.452 × 10−2	4.620 × 10−3–9.440 × 10−3	≤4.610 × 10−3	
9.5	≥2.099 × 10−2	1.533 × 10−2–2.098 × 10−2	9.970 × 10−3–1.532 × 10−2	4.870 × 10−3–9.960 × 10−3	≤4.860 × 10−3	
10.0	≥2.208 × 10−2	1.613 × 10−2–2.207 × 10−2	1.049 × 10−2–1.612 × 10−2	5.130 × 10−3–1.048 × 10−2	≤5.120 × 10−3	

Inbreeding Increments and Inbreeding Coefficients in Pigeon Groups Under Different Retention Modes

Inbreeding increments decreased with increasing population size for random-reserved and family-equal-reserved selection (Figure 2A). In addition, when the population effective content was the same, the inbreeding increment of random-reserved selection was greater than that for family-equal-reserved selection.Figure 2 Inbreeding increments and inbreeding coefficients under different retention methods. (A) Inbreeding increment under different retention methods. (B) Inbreeding coefficients of different generations of different populations under random-reserved selection. (C) The inbreeding coefficient of each generation of different populations under family-equal-reserved selection.

Figure 2

The inbreeding coefficient gradually decreased with increasing population size (Figure 2B and C). In the case of random-reserved selection, the effective population content was 10 pigeons first reached an inbreeding coefficient of 0.1 in the second generation, while the effective population content was 64 pigeons only reached the same inbreeding coefficient in the 13th generation. In the case of family-equal-reserved selection among different lines, the effective population content was 10 pigeons first reached an inbreeding coefficient of 0.1 in the fourth generation, while the effective population content was 64 pigeons reached the same coefficient in the 26th generation.

For the same generation interval, a larger population had a lower average inbreeding increment and better species preservation effect. The average inbreeding increment of random-reserved selection was twice as large as that for family-equal-reserved selection (Figure 2), indicating that family-equal-reserved selection has a better conservation effect than random-reserved selection.

DISCUSSION

Highly selected pigeon breeds are the basis for the development of the modern pigeon industry, which is largely dependent on a few breeds or types with excellent performance. This has resulted in a substantial threat to many local breeds and types with certain characteristics (Jackson et al., 2022; Wilson, 2003; Fernandes et al., 2023). In addition, the diversification of some breeds, along with natural disasters and environmental impacts, especially the discriminate environmental-protection policies in some economies, has led to the withdrawal of many small- and medium-scale pigeon farms from the breeding industry. Intensive production and highly selective breeding have continued to reduce the available genetic variance.

Long-term selection will eventually exhaust the genetic variance within varieties and the selection limit will be reached, highlighting the need to preserve genetic variation to allow “limits” to be breached when they occur. In addition, the 1-sided pursuit of yield in the breeding process has resulted in the creation of high-yield varieties with serious defects in other traits, which may in contrast be advantages of other poorly preserved varieties. The development of human societies and economies will impose new requirements in terms of pigeon consumption, and the current economic characteristics may not be suitable in the future, while characteristics that are presently considered desirable may not be so in the future.

In the case of pigeons, it is not possible to cryopreserve embryos or oocytes, mainly because of their large size, high lipid content, and polar organization (vegetal and animal poles) (Sun et al., 2022). In addition, the limitations of ecological, geographical, and technical conditions mean that in situ conservation is still the main way of poultry preservation, and the practical conservation of pigeon genetic resources is frequently achieved through population preservation.

One reason for preserving rare or native pigeon breeds is that these breeds may meet the specific requirements of the local terrain or climate, or may produce typical regional products. According to research data, at the end of 2020, China's breeding pigeon inventory is about 46 million pairs, and in 2020, about 490 million commercial pigeons will be listed, accounting for more than 80% of the world's total (Tang et al., 2021). There are more than 20 breeds of pigeons raised in China, including Shiqi pigeon, Talimu pigeon, Taihu Chizi pigeon, Tianxiang Pigeon No. 1 matching line, Suwei pigeon No. 1 matching line and White royal pigeon, Silver royal pigeon, grey royal pigeon, European pigeon, European pigeon I1 and European pigeon III (Zhu et al., 2024). However, the ensuing problem is that China's native meat pigeon breeds are eliminated, or in the breeding process, they are selected to cross breed with Mimas to breed new varieties. At the same time, it is necessary to maintain the genetic diversity of more widely used varieties, given that varieties that are widely used can suffer from inherited diseases such as deformities or dysfunctions caused by inbreeding. In addition, it is crucial to maintain genetic diversity as a toolbox for flock breeding, to adapt to possible future breeding targets. The main goal of species conservation planning is to preserve the genetic diversity of the population to the maximum extent (Cervantes and Meuwissen, 2011).

The Convention on Biological Diversity was adopted at the 1992 Earth Summit, with the objectives of conserving biological diversity, and promoting the sustainable use of natural resources and the fair and equitable sharing of the benefits that arise out of the use of genetic resources (Woelders et al., 2006). Countries throughout the world have different degrees of understanding of conservation, and many international organizations and countries have formulated and implemented various conservation management methods and measures.

The pigeon was likely domesticated at least 5,000 yr ago in the Middle East and/or Mediterranean region, making it one of the oldest avian domesticates, and also the most phenotypically diverse (Price, 2002; Stringham et al., 2012). In scientific research, the genetic diversity of pigeons offer several advantages as a model to understand the molecular basis of avian and vertebrate diversity (Domyan and Shapiro, 2017). (1) After thousands of years of breeding, the degree of variation between pigeon breeds can approach the amount and extent of differences normally observed between different species. (2) Pigeons are easy to breed and can be successfully interbred between almost all breeds to produce fertile offspring. (3) Classical studies show that the genetic architecture of many traits in pigeons is probably oligogenic, thereby increasing the chances of mapping and cloning the genes responsible for differences among breeds. Furthermore, relatively complex traits can sometimes be genetically teased apart into discrete components, thereby facilitating mapping of each component. (4) Many of the variable traits of pigeons are also variable in birds, providing a key entry point in the search for genes that control variation in the wild. (5) Many derived traits in domestic pigeons are constructive rather than regressive. (6) Phenotypic convergence is common in breeds, that is, traits that are phenotypically identical are not necessarily controlled by the same genes. Understanding how these similarities arise is an area of intense interest in evolutionary developmental biology and genetics.

Inbreeding and effective population size are useful for long-term management of genetic variability and monitoring of genetic trends. There are many ways in which a flock can measure genetic variation and loss of diversity, but when genealogical records are known, the traditional way is to calculate the inbreeding coefficient, which becomes more effective the more generations involved in the genealogical record (Leroy, 2011). The earliest work in conservation of endangered species focused on breeding in captivity to increase population sizes and for eventual release back into the wild. However, demographic security and the maintenance of genetic diversity can sometimes be at odds, as genetic diversity is derived from Ne (Athrey et al., 2018). Ne can be defined as the size of an ideal population that experiences the same amount of genetic drift or inbreeding as the actual (census) population (Wright, 1948). The results of this study also indicated that when the Ne of the flock was small, the rate of genetic diversity reduction was faster, which was consistent with the results of Montgomery et al (2000). Long-term conservation still depends mainly on population size (Hoffmann et al., 2017; Iizuka, 2010; Ragab et al., 2015). The main reason is that the smaller the population size, the greater the effect of genetic drift (Hubert et al., 2000). When the population size reaches a certain critical value, the effect of genetic drift on the population genetic structure is the first, and factors such as selection, mutation and migration cannot antagonize the effect of genetic drift (Falconer et al., 1990; Oldenbroek, 2007).

During the process of species preservation, the preserved population is also a closed population of limited size. It is therefore necessary to take scientific and reasonable measures to reduce the risk of gene loss or fixation caused by random genetic drift, to improve the effect of gene bank species preservation (Wang, 2004). An increase in flock size would reduce the increment of inbreeding, leading to a better preservation effect.

For breed conservation planning, the main conservation goal is to preserve the genetic diversity of the population to the maximum extent (Cervantes and Meuwissen, 2011). Generally, the breeding life of domestic animals is 50 to 150 yr, and the 1% inbreeding increment per generation is equivalent to the Ne of 50 animals, which is the minimum population size required for short-term breeding (Food and Agriculture Organization of the United Nations, 1998). Franklin (1980) proposed that the increase in inbreeding should be limited to 1% per generation, to eliminate the decline caused by inbreeding and protect the population from extinction. The currently accepted conservation goal is to preserve 90% of the original genetic diversity for at least 100 yr (Soulé et al., 1986).

The generation interval itself does not directly affect the increment in average inbreeding coefficient, but is closely related to the rate of change of the population genetic structure within a certain period of time (Anthony et al., 1996; Rahim et al., 2023). Extending the generation interval is therefore beneficial in terms of the long-term conservation of genetic resources, and can effectively slow down genetic changes in pigeon groups. In actual production and scientific research, the generation intervals of all kinds of poultry were 1.5 yr for chicken, 2 yr for duck and 3 yr for goose (NY/T2996-2016, 2016). In the breeding process of pigeons, in order to speed up the genetic progress, the generation interval is often shortened by the following methods: (1) shorten the service life of the breeding pigeons as much as possible; (2) On the premise of ensuring the accuracy of selection, select the seed selection method with a short generation interval. For example, breeding pigeons are genetically assessed only on the production performance and other information of the first 2 pigeons produced in the litter; (3) Implement early breeding. For the in-situ preservation of pigeons, there is a lack of another implementation method. According to the results of this study, we can find that in the conservation of pigeons, the generation interval should be extended appropriately, so as to reduce the increase of the inbreeding coefficient of the population.

According to the theory of population genetics, a large population and random breeding and mating are required to reduce the effects of mutation, selection, migration, and genetic drift (Molina and Earn, 2018). Conserved populations are usually closed limited populations, and even in the absence of systematic factors affecting the genetic structure of the population, random drift of population gene frequencies will be caused by gamete sampling errors caused by the small flock size: the frequency of homozygosity may be increased and heterozygosity decreased, or alleles may become fixed as homozygous, with the other gene lost. It is almost impossible to preserve every gene in a limited population for a long time without losing any genes, and we can only try to reduce the rate and probability of gene loss or fixing by reasonable measures. It is therefore necessary to minimize the effect of random genetic drift on the population; the size of this effect can be predicted from the available population content, but the direction of its effect is uncertain. In the case of random-reserved selection of chickens, ducks and geese, the minimum Ne of safety grade was 650, 488, and 325 (NY/T2996-2016, 2016), respectively, while the number of pigeons was 325. The number of pigeons kept is the same as that of geese, mainly because pigeons are “monogamous” and, in addition, they live at shorter intervals than geese.

Compared with random-reserved selection, the population effective content was higher and the population inbreeding increment was lower with family-equal-reserved selection. Random-reserved selection is not possible in a large breeder population, because different individuals have different social positions within the flock (Carleial et al., 2020; Craig et al., 1977).For pigeon conservation, the same numbers of species should thus be retained from each family; however, random mating was not necessary, because family-equal-reserved selection avoids mating between full and/or half siblings effectively reduced the inbreeding rate and improved the conservation effect (Casillas and Barbadilla, 2017). In the case of family-equal-reserved selection of chickens, ducks and geese, the minimum Ne of safety grade was 325, 244, and 163 (NY/T2996-2016, 2016), respectively, while the number of pigeons was 163.

If the population size decreases drastically within a given generation, it will have a profound effect on the genetic structure of the population, creating a so-called bottleneck effect (Nitschke et al., 2023). The increase in average inbreeding depends mainly on the generation population size; the smaller the effective population size, the more serious the population genetic drift (Martins et al., 2011). This effect will persist long after the population has returned to its original state. Increases, decreases, or random fluctuations in population size between generations can seriously affect the rate of increase in inbreeding, and maintaining a constant population size over successive generations is thus an important aim of population conservation (Keeling et al., 2017; Sellier, 2000). These conditions reduce the rate of increase in inbreeding increment and help to avoid the bottleneck effect (Athrey et al., 2018), which is beneficial in terms of species preservation. The current status of preservation, which must utilize live animal stocks, has contributed to the loss of genetic resources (Fulton, 2006). Future preservation utilizing gamete or embryo cryopreservation will be possible once appropriate technologies are developed. With the development of biological technology, the application of modern biotechnology to explore the preservation of genetic material such as primitive germ cells and blood (Lone et al., 2019) can further supplement the protection of poultry genetic resources (Manyelo et al., 2020).

CONCLUSION

There are many factors that affect the breeding of pigeons. In order to keep the genetic structure of pigeons stable, it is necessary to reduce the factors that break the Hardy-Weinberg balance and maintain sufficient number of pigeons. The current experimental results indicate several measures that can be taken to ensure the stability of the genetic structure of a certain breed of pigeons: (1) establish and preserve the number of pigeon groups corresponding to the “safe” level in the improved breeding base. The lowest Ne was 325, and the generation interval was longer than 1.5 yr. (2) when breeding in each generation, the family-equal-reserved selection should be implemented, to try to maintain the same flock size in each generation and reduce the bottleneck effect; (3) appropriate extension of the generation interval; (4) generally avoid selection within the preserved population, and only combine species preservation and breeding when there is no alternative.

Appendix Supplementary materials

Image, application 1

ACKNOWLEDGMENTS

This work was supported by the Agriculture Research System of Shanghai (202212 ); SAAS Program for Excellent Research Team (2022-021 ); Shanghai Agriculture Applied Technology Development Program (2018-02-08-0012-FO1546 ).

Author contributions: All authors were equally contributed in writing this article. All authors reviewed and approved the final version of the manuscript.

DISCLOSURES

The authors declared that they have no conflicts of interest to this work.

Supplementary material associated with this article can be found in the online version at doi:10.1016/j.psj.2024.104091.
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