유성생식, 무성생식, 생물의 성, 유전적 변이, 돌연변이, 자연 선택, 진화
Sexual reproduction, asexual reproduction, sex of organisms, genetic variation, mutation, natural selection, evolution
유성생식
有性生殖
Sexual Reproduction
유성생식이란, 암컷과 수컷의 생식세포가 유전자를 결합하여 새로운 자손을 생산하는 생식방법이다. 유성생식의 시작으로 성의 시작과 탄생이 이루어졌다.
약 45억년 전 초기 지구의 바다는 5억년뒤인 40억년쯤 최초의 생명체가 탄생한 장소로 단세포 생물이 무성생식으로 번식하기에 적당한 조건이었는데, 이때는 성이 미분화된 상태였으므로 무성생식을 통해 자손을 번식했었다. 그러나 시간이 지나면서 약 10억년 전에 지구환경의 급격한 변화로 초기 생명체(단세포 생물)들의 생존 및 번식이 어려운 조건으로 바뀌게 되었고, 이에 따라 생존을 위한 세포간의 유전자 교환을 통한 유성생식이 생겨 났다. 두 세포간 유전자가 합쳐지면서 독특한 자식들이 등장했는데 이 중 더 우수한(즉 환경에 맞는) 자식 세포가 등장해 진화를 가속화 했다. 그래서 단세포 생물의 유성생식은 다세포 생물과 좀 다르다. 생물학적 성이 2개 내외인 다세포 생물과 달리 성이 10개가 넘는 단세포 생물도 있고 환경이 좋으면 그냥 복제하여 무성생식을 했다.
이러한 유성 생식은 후에 세포간 결합(협동)이 유발되면서 여러 세포로 구성된 생명체인 다세포 생물이 탄생하게 되었다. 지속적인 생존경쟁을 거치며 세포기능이 다양화되었고 이것은 곧 생식세포를 형성하게 되었다. 다세포 생물의 생식세포의 형성으로 암컷과 수컷의 분화 및 독립이 이루어졌고 비로소 이분법적 성의 탄생이 이루어지게 되었다. 초창기 다세포 생물들은 조상인 단세포 생물처럼 환경이 좋으면 그냥 자신을 복제하는 무성생식을 했지만 다세포 생물의 몸구조가 복잡해지면서 반드시 유성생식을 하게끔 진화하게 된다. 이에 따라 시간이 지나면서 더욱 다양하고 우수한 유전자 확보를 위한 유성생식의 발전 및 진화를 이루었고 현재에 이르게 되었다.
무성생식과의 비교
유성생식 결과 부모 양쪽의 유전자 조합으로 유전적 다양성을 획득함으로서, 한 개체가 단독으로 자손을 생산해서 세대 간에 유전자 차이가 상대적으로 적을 수밖에 없는 무성생식과 대비된다.
무성생식은 짝짓기 과정 없이 번식할 수 있으므로 얼핏 효율적으로 보이나, 사실상 클론을 만드는 것이므로 유전적 다양성을 확보하기가 그만큼 어렵다. 진화를 전적으로 돌연변이나 수평전파에 의존하므로 이는 종 전체의 환경 적응력이 낮아짐을 뜻한다. 그렇기에 동물과 식물들을 비롯한 절대다수의 다세포 생물은 유성생식을 한다. 심지어 일부 단세포 생물도 상황에 따라선 유성생식을 하며, 필요에 따라 유전자만 교환하는 접합도 한다.
참고로 꿀벌 등 일부 생물은 유성생식과 무성생식을 둘 다 할 수 있으며, 둘 다 종족의 유지에 필수적이다.
생물의 성
생명에게는 너무나 자연스러워서 잘 생각하지 않지만, 사실 이상한 것이 있다. 그것은 곧 ‘성’이다. 왜 생물에게는 암컷, 수컷 같은 성이 생겼을까? 또 왜 세 개가 아니라 두 개 일까? 왜 생물은 유성생식을 할까? 이러한 질문의 생물학에서 아직도 명확한 답이 나오지 않은 근본적인 질문이다. 다만 성의 발생과 유성생식의 이점을 설명하는 여러 가설이 있다. 무엇이 있는지 살펴보자.
먼저 유성생식이란 암컷의 생식세포인 난자와 수컷의 생식세포인 정자가 융합해 자손을 낳는 것을 말한다. 하지만 자연에는 무성생식도 있다. 한 개체에서 새로운 개체가 자라 나오거나 몸이 몇 개의 조각으로 나눠진 뒤 없어진 몸의 일부가 다사 생장하는 것이다. 이러한 무성생식은 유성생식보다 더 유리하다. 번식을 위해 짝을 찾아야 하는 번거로움도 없고 기하급수적으로 자손의 수를 늘릴 수도 있다. 유성생식이 가진 이런 불리함에도 불구하고 먼 과거의 어느 날 양성이 생기고 유성생식이 진화했다면 분명 특정 조건에서 무성생식을 압도하는 이점이 있었을 것이다.
성은 유전적 다양성을 늘린다
가장 첫 번째로 제시된 가설은 유전적 다양성을 증가시켜 환경에 잘 적응하기 위한 것이라는 설명이다. 무성생식은 원 개체의 유전자가 세대를 내려가며 똑같이 복제되는 것이다. 반면 유성생식은 무엇보다 두 개체로부터 유전물질을 혼합해 새로운 개체를 만드는 과정이다. 부모의 유전자가 섞이므로 세대를 내려갈수록 유전적 다양성은 증가한다. 이런 다양성은 자연선택이 작용할 수 있는 특성들을 늘려준다.
자연의 생물에는 개체마다 다양한 변이가 있고, 이런 변이 중 생존과 번식에 유리한 것이 자연선택되어 자손에게 전해진다. 무성생식에서는 유전자가 그대로 복제되기 때문에 돌연변이가 발생할 가능성이 적지만 유성생식에서는 언제나 변이가 일어난다. 물론 이런 변이가 언제나 이로운 것은 아니지만 그래도 만에 하나 그때 그 환경에 잘 맞는 변이가 있다면 유전자 입장에서는 좋은 것이다.
성은 기생생물을 막고 복제 오류를 교정한다
두 번째 가설은 유성생식은 기생생물을 막기 위해 진화했다고 설명한다. 이 가설은 유성생식이 다양성을 증가시키기 위해 진화했다는 생각에는 동의한다. 하지만 그 다양성은 기생생물을 막기 위해 필요한 것이라고 주장한다. 다양한 생물이 공존하는 자연계에는 서로가 서로를 이용하기 위한 진화적 군비경쟁이 일어난다. 기생생물은 언제나 숙주를 이용하고자 하고 숙주는 이를 막으려 한다. 기생생물은 숙주의 유전자를 탈취해 자기자신을 복제한다. 그때 숙주가 쓸 수 있는 방법 중 하나가 유성생식을 해서 기생생물이 쉽게 침투할 수 없도록 하는 것이다.
우리가 잘 알다시피 유전적 다양성이 없으면 환경이 급변하거나 세균, 바이러스가 침투하면 개체군 전체가 몰살할 수 있다. 공장식 축산이 문제가 되는 이유는 자연 상태와 달리 동물들의 유전적 다양성이 없어 감염병에 취약하기 때문이다. 기생생물이 손쉽게 숙주를 지배할 수 있는 것이다. 따라서 무성생식은 비용이 적게 드나 한순간의 변화로 모든 구성원이 위험에 처할 수 있기에 다소 손해를 감수하더라도 유성생식을 하는 방향으로 진화했다는 것이다.
세 번째 가설은 성이 유전적 다양성을 늘리기보다는 오히려 제한하기 위해 진화했다고 말한다. 생물을 이루는 DNA는 끊임없이 복제되면서 잘못 복제되는 오류가 발생하기도 한다. 그렇기에 DNA에는 이런 오류를 교정하는 시스템이 있다. 하지만 교정으로도 복구가 안 되는 돌연변이는 늘 있게 마련이다. 무성생식하는 동물은 이 돌연변이가 자식에게 전부 전달되므로 해로운 돌연변이가 세포에 점점 누적되어가는 것을 막을 수 없다. 그러나 유성생식을 한다면 설사 해로운 돌연변이가 발생했다 하더라도 다음 세대에 유전자가 섞으므로 돌연변이를 제거할 수 있다.
성이 왜 존재하는지에 대해서는 진화생물학자, 유전학자, 분자생물학자마다 의견이 다르다. 위에서 소개한 세 가지 가설 외에도 다른 가설도 있다. 그러나 중요한 것은 세 가지 가설이 모두 독립적이라고 생각할 필요는 없다는 것이다. 유성생식은 무성생식보다 번거롭고 비용이 많이 드는 방식이므로 어느 한 가지 이점만으로 선택된 것은 아닐 수도 있다. 유성생식은 유전적 다양성을 늘려 환경에 적응하게 하는 동시에 바이러스 같은 기생생물을 막고 DNA의 오류를 교정하는 역할까지 다양한 이점을 주었기에 진화한 것일지도 모른다.
유전적 변이(遺傳的變異, 영어: genetic variation)
개인 간의 DNA 차이 또는 집단 간의 차이이다. 유전적 변이의 여러 원인에는 돌연변이와 유전적 재조합이 있다. 돌연변이는 유전적 변이의 궁극적인 원인이지만 유성 생식 및 유전자 부동과 같은 다른 메커니즘도 이에 기여한다.
개인 간의 차이
유전적 변이는 여러 수준에서 확인할 수 있다. 유전적 변이를 식별하는 것은 양적 특성(연속적으로 변하고 많은 유전자에 의해 코딩되는 특성(예: 개의 다리 길이) 또는 개별 특성(불연속 범주에 속하고 하나 또는 몇 개의 유전자(예: 특정 꽃의 흰색, 분홍색 또는 붉은색 꽃잎 색상))이다.
유전적 변이는 또한 단백질 전기영동과정을 이용하여 효소 수준에서의 변이를 조사함으로써 확인될 수 있다. 다형성 유전자는 각 유전자 좌위에 하나 이상의 대립 유전자를 가지고 있다. 곤충과 식물에서 효소를 코딩하는 유전자의 절반은 다형성일 수 있지만, 다형성은 척추동물에서 덜 일반적이다.
궁극적으로 유전자 변이는 유전자의 뉴클레오티드 염기 순서의 변이에 의해 발생한다. 이제 새로운 기술을 통해 과학자들은 이전에 단백질 전기영동으로 감지했던 것보다 훨씬 더 많은 유전적 변이를 식별한 DNA의 염기서열을 직접 확인할 수 있다. DNA 검사는 유전자의 암호화 영역과 비암호화 인트론 영역 모두에서 유전적 변이를 보여주었다.
유전적 변이는 DNA 서열의 뉴클레오티드 순서의 변이가 그 DNA 서열에 의해 암호화된 단백질의 아미노산 순서의 차이를 초래하고 아미노산 서열의 결과적인 차이가 모양에 영향을 미치는 경우 표현형 변이를 초래할 것이다. 따라서 효소의 기능이 달라진다.
집단 간의 차이
지리적 변이는 다른 위치에서 온 개체군의 유전적 차이를 의미한다. 이것은 자연 선택 또는 유전자 부동에 의해 발생한다.
측정
집단 내의 유전적 변이는 일반적으로 다형성 유전자 좌의 백분율 또는 이형접합 개체의 유전자 좌의 백분율로 측정된다.
출처
홍합 Donax variabilis 의 가변성 범위
무작위 돌연변이는 유전적 변이의 궁극적인 원인이다. 돌연변이는 드물고 대부분의 돌연변이는 중립적이거나 유해하지만 어떤 경우에는 새로운 대립 유전자가 자연 선택에 의해 선호될 수 있다. 배수성은 염색체 돌연변이의 한 예이다. 배수성은 유기체가 3개 이상의 유전적 변이(3n 이상) 세트를 갖는 상태이다.
감수 분열 동안 교차(유전적 재조합) 및 무작위 분리는 새로운 대립 유전자 또는 대립 유전자의 새로운 조합을 생성할 수 있다. 또한, 무작위 수정도 변이에 기여한다. 변형 및 재조합은 전이 가능한 유전 요소, 내인성 레트로바이러스, LINE, SINE 등에 의해 촉진될 수 있다. 다세포 유기체의 주어진 게놈에 대해 유전적 변이는 체세포에서 획득되거나 생식선을 통해 유전될 수 있다.
양식
유전적 변이는 유전적 변화를 뒷받침하는 게놈 변이의 크기와 유형에 따라 여러 형태로 나눌 수 있다. 소규모 서열 변이(<1kb(킬로베이스))에는 염기쌍 치환 및 삽입결실이 포함된다. 대규모 구조적 변이 (>1kb)는 복제 수 변이 ( 손실 또는 증가 ) 또는 염색체 재배열 ( 전좌, 역전 또는 분절 후천적 단일친 이염색체 )일 수 있다. 이식 가능한 요소 및 내인성 레트로바이러스에 의한 유전적 변이 및 재조합은 때때로 숙주 게놈에서 유전적 신규성을 생성하는 다양한 지속성 바이러스 및 이들의 결함에 의해 보완된다. 전체 염색체 또는 게놈의 수치적 변이는 배수성 또는 이수성일 수 있다.
인구 유지
다양한 요인들이 집단의 유전적 변이를 유지한다. 잠재적으로 해로운 열성 대립유전자는 이배체 유기체 집단의 이형접합 개체에서 선택에서 숨겨질 수 있다(열성 대립유전자는 덜 흔한 동형접합 개체에서만 발현됨). 자연 선택은 또한 균형 잡힌 다형성에서 유전적 변이를 유지할 수 있다. 균형 잡힌 다형성은 이형 접합체가 선호되거나 선택이 빈도 의존적일 때 발생할 수 있다.
RNA 바이러스
교정 메커니즘의 부족으로 인한 높은 돌연변이 비율은 RNA 바이러스 진화에 기여하는 유전적 변이의 주요 원인으로 보인다. 유전자 재조합은 또한 RNA 바이러스 진화의 기초가 되는 유전적 변이를 생성하는 데 중요한 역할을 하는 것으로 나타났다. 다수의 RNA 바이러스는 적어도 2개의 바이러스 게놈이 동일한 숙주 세포에 존재할 때 유전적 재조합이 가능하다. RNA 재조합은 Picornaviridae ((+)ssRNA)(예: 폴리오바이러스) 간의 게놈 구조와 바이러스 진화과정을 결정하는 주요 원동력으로 보인다. Retroviridae ((+)ssRNA)(예: HIV), RNA 게놈의 손상은 유전적 재조합의 한 형태인 가닥 전환에 의한 역전사 동안 회피되는 것으로 보인다.
이러한 재조합은 코로나바이러스과 ((+)ssRNA)에서도 발생한다(예: 사스). RNA 바이러스의 재조합은 게놈 손상에 대처하기 위한 적응으로 보이다. 재조합은 같은 종의 동물 바이러스 사이에서 드물게 발생할 수 있지만 계통이 다르다. 생성된 재조합 바이러스는 때때로 사람에게 감염을 일으킬 수 있다
변이와 자연 선택에 의한 생물의 진화
1. 변이와 자연 선택에 의한 생물의 변화
주어진 환경에 적응하여 살아남는 데 유리한 변이를 가진 개체는 살아남아 자손을 남기고, 이러한 자연 선택 과정이 오랫동안 반복되면서 생물의 진화가 일어난다.
2. 변이와 진화
① 변이
같은 종에 속한 개체들 사이에서 나타나는 형태, 습성, 기능 등의 형질의 차이로, 진화가 일어나는 원동력이 된다.
② 유전적 변이가 나타나는 까닭
유전적 변이는 오랫동안 축적된 돌연변이와 유성 생식 과정에서 생식세포 분열의 다양한 유전자 조합으로 발생한다.
※ 돌연변이 : DNA의 유전 정보에 변화가 생겨 부모에게 없던 형질이 자손에게 나타나는 것이다. → 돌연변이는 새로운 유전자를 만들어 내며, 자손에게 유전된다.
● 붉은색 딱정벌레 무리의 자손 중에 초록색 딱정벌레가 나타났다. → 새로운 변이의 출현
● 돌연변이로 새롭게 초록색 유전자가 나타났으며, 초록색 딱정벌레는 무리 내에서 교배하여 자손에게 초록색 유전자를 물려준다. → 딱정벌레 집단의 유전적 변이가 다양해진다.
※ 생식세포의 다양한 유전자 조합
유성 생식을 하는 생물은 생식세포 분열에 의해 생식세포를 형성하는데, 이 과정에서 유전자 조합이 다양한 생식세포를 형성한다.
● 흰색 털과 갈색 털을 가진 부모 사이에서 얼룩무늬 강아지가 태어났다.
● 얼룩무늬 강아지는 흰색 털 유전자와 갈색 털 유전자를 모두 가진다. → 얼룩무늬 강아지는 자손에게 흰색 털 유전자와 갈색 털 유전자를 물려줄 수 있다.
● 세대를 거듭하면서 자손의 유전자 조합이 다양해진다. → 변이가 다양해진다.
Evolution of sexual reproduction
Evolution of sexual reproduction describes how sexually reproducing animals, plants, fungi and protists could have evolved from a common ancestor that was a single-celled eukaryotic species.[1][2][3] Sexual reproduction is widespread in eukaryotes, though a few eukaryotic species have secondarily lost the ability to reproduce sexually, such as Bdelloidea, and some plants and animals routinely reproduce asexually (by apomixis and parthenogenesis) without entirely having lost sex. The evolution of sexual reproduction contains two related yet distinct themes: its origin and its maintenance. Bacteria and Archaea (prokaryotes) have processes that can transfer DNA from one cell to another (conjugation, transformation, and transduction[4]), but it is unclear if these processes are evolutionarily related to sexual reproduction in Eukaryotes.[5] In eukaryotes, true sexual reproduction by meiosis and cell fusion is thought to have arisen in the last eukaryotic common ancestor, possibly via several processes of varying success, and then to have persisted.[6]
Since hypotheses for the origin of sex are difficult to verify experimentally (outside of evolutionary computation), most current work has focused on the persistence of sexual reproduction over evolutionary time. The maintenance of sexual reproduction (specifically, of its dioecious form) by natural selection in a highly competitive world has long been one of the major mysteries of biology, since both other known mechanisms of reproduction – asexual reproduction and hermaphroditism – possess apparent advantages over it. Asexual reproduction can proceed by budding, fission, or spore formation and does not involve the union of gametes, which accordingly results in a much faster rate of reproduction compared to sexual reproduction, where 50% of offspring are males and unable to produce offspring themselves. In hermaphroditic reproduction, each of the two parent organisms required for the formation of a zygote can provide either the male or the female gamete, which leads to advantages in both size and genetic variance of a population.
Sexual reproduction therefore must offer significant fitness advantages because, despite the two-fold cost of sex (see below), it dominates among multicellular forms of life, implying that the fitness of offspring produced by sexual processes outweighs the costs. Sexual reproduction derives from recombination, where parent genotypes are reorganised and shared with the offspring. This stands in contrast to single-parent asexual replication, where the offspring is always identical to the parents (barring mutation). Recombination supplies two fault-tolerance mechanisms at the molecular level: recombinational DNA repair (promoted during meiosis because homologous chromosomes pair at that time) and complementation (also known as heterosis, hybrid vigour or masking of mutations).
Historical perspective
Reproduction, including modes of sexual reproduction, features in the writings of Aristotle; modern philosophical-scientific thinking on the problem dates from at least Erasmus Darwin (1731–1802) in the 18th century.[7] August Weismann picked up the thread in 1885, arguing that sex serves to generate genetic variation, as detailed in the majority of the explanations below.[8] On the other hand, Charles Darwin (1809–1882) concluded that the effect of hybrid vigor (complementation) "is amply sufficient to account for the … genesis of the two sexes".[9] This is consistent with the repair and complementation hypothesis, described below. Since the emergence of the modern evolutionary synthesis in the 20th century, numerous biologists including W. D. Hamilton, Alexey Kondrashov, George C. Williams, Harris Bernstein, Carol Bernstein, Michael M. Cox, Frederic A. Hopf and Richard E. Michod – have suggested competing explanations for how a vast array of different living species maintain sexual reproduction.
Advantages of sex and sexual reproduction
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The concept of sex includes two fundamental phenomena: the sexual process (fusion of genetic information of two individuals) and sexual differentiation (separation of this information into two parts). Depending on the presence or absence of these phenomena, all of the existing forms of reproduction can be classified as asexual, hermaphrodite or dioecious. The sexual process and sexual differentiation are different phenomena, and, in essence, are diametrically opposed. The first creates (increases) diversity of genotypes, and the second decreases it by half.
Reproductive advantages of the asexual forms are in quantity of the progeny, and the advantages of the hermaphrodite forms are in maximal diversity. Transition from the hermaphrodite to dioecious state leads to a loss of at least half of the diversity. So, the primary challenge is to explain the advantages given by sexual differentiation, i.e. the benefits of two separate sexes compared to hermaphrodites rather than to explain benefits of sexual forms (hermaphrodite + dioecious) over asexual ones. It has already been understood that since sexual reproduction is not associated with any clear reproductive advantages over asexual reproduction, there should be some important advantages in evolution.[10][better source needed]
Advantages due to genetic variation, DNA repair and genetic complementation
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See also: Hill–Robertson effect
For the advantage due to genetic variation, there are three possible reasons this might happen. First, sexual reproduction can combine the effects of two beneficial mutations in the same individual (i.e. sex aids in the spread of advantageous traits) without the mutations having to have occurred one after another in a single line of descendants.[11] [unreliable source?] Second, sex acts to bring together currently deleterious mutations to create severely unfit individuals that are then eliminated from the population (i.e. sex aids in the removal of deleterious genes). However, in organisms containing only one set of chromosomes, deleterious mutations would be eliminated immediately, and therefore removal of harmful mutations is an unlikely benefit for sexual reproduction. Lastly, sex creates new gene combinations that may be more fit than previously existing ones, or may simply lead to reduced competition among relatives.
For the advantage due to DNA repair, there is an immediate large benefit of removing DNA damage by recombinational DNA repair during meiosis (assuming the initial mutation rate is higher than optimal[12]), since this removal allows greater survival of progeny with undamaged DNA. The advantage of complementation to each sexual partner is avoidance of the bad effects of their deleterious recessive genes in progeny by the masking effect of normal dominant genes contributed by the other partner.[13][14]
The classes of hypotheses based on the creation of variation are further broken down below. Any number of these hypotheses may be true in any given species (they are not mutually exclusive), and different hypotheses may apply in different species. However, a research framework based on creation of variation has yet to be found that allows one to determine whether the reason for sex is universal for all sexual species, and, if not, which mechanisms are acting in each species.
On the other hand, the maintenance of sex based on DNA repair and complementation applies widely to all sexual species.
Protection from major genetic mutation
In contrast to the view that sex promotes genetic variation, Heng,[15] and Gorelick and Heng[16] reviewed evidence that sex actually acts as a constraint on genetic variation. They consider that sex acts as a coarse filter, weeding out major genetic changes, such as chromosomal rearrangements, but permitting minor variation, such as changes at the nucleotide or gene level (that are often neutral) to pass through the sexual sieve.
Novel genotypes
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This diagram illustrates how sex might create novel genotypes more rapidly. Two advantageous alleles A and B occur at random. The two alleles are recombined rapidly in a sexual population (top), but in an asexual population (bottom) the two alleles must independently arise because of clonal interference.
Sex could be a method by which novel genotypes are created. Because sex combines genes from two individuals, sexually reproducing populations can more easily combine advantageous genes than can asexual populations. If, in a sexual population, two different advantageous alleles arise at different loci on a chromosome in different members of the population, a chromosome containing the two advantageous alleles can be produced within a few generations by recombination. However, should the same two alleles arise in different members of an asexual population, the only way that one chromosome can develop the other allele is to independently gain the same mutation, which would take much longer. Several studies have addressed counterarguments, and the question of whether this model is sufficiently robust to explain the predominance of sexual versus asexual reproduction remains.[17]: 73–86 [16][18]
Ronald Fisher suggested that sex might facilitate the spread of advantageous genes by allowing them to better escape their genetic surroundings, if they should arise on a chromosome with deleterious genes.
Supporters of these theories respond to the balance argument that the individuals produced by sexual and asexual reproduction may differ in other respects too – which may influence the persistence of sexuality. For example, in the heterogamous water fleas of the genus Cladocera, sexual offspring form eggs which are better able to survive the winter versus those the fleas produce asexually.
Increased resistance to parasites
One of the most widely discussed theories to explain the persistence of sex is that it is maintained to assist sexual individuals in resisting parasites, also known as the Red Queen Hypothesis.[19][17]: 113–117 [20][21][22]
When an environment changes, previously neutral or deleterious alleles can become favourable. If the environment changed sufficiently rapidly (i.e. between generations), these changes in the environment can make sex advantageous for the individual. Such rapid changes in environment are caused by the co-evolution between hosts and parasites.
Imagine, for example that there is one gene in parasites with two alleles p and P conferring two types of parasitic ability, and one gene in hosts with two alleles h and H, conferring two types of parasite resistance, such that parasites with allele p can attach themselves to hosts with the allele h, and P to H. Such a situation will lead to cyclic changes in allele frequency – as p increases in frequency, h will be disfavoured.
In reality, there will be several genes involved in the relationship between hosts and parasites. In an asexual population of hosts, offspring will only have the different parasitic resistance if a mutation arises. In a sexual population of hosts, however, offspring will have a new combination of parasitic resistance alleles.
In other words, like Lewis Carroll's Red Queen, sexual hosts are continually "running" (adapting) to "stay in one place" (resist parasites).
Evidence for this explanation for the evolution of sex is provided by comparison of the rate of molecular evolution of genes for kinases and immunoglobulins in the immune system with genes coding other proteins. The genes coding for immune system proteins evolve considerably faster.[23][24]
Further evidence for the Red Queen hypothesis was provided by observing long-term dynamics and parasite coevolution in a "mixed" (sexual and asexual) population of snails (Potamopyrgus antipodarum). The number of sexuals, the number asexuals, and the rates of parasite infection for both were monitored. It was found that clones that were plentiful at the beginning of the study became more susceptible to parasites over time. As parasite infections increased, the once plentiful clones dwindled dramatically in number. Some clonal types disappeared entirely. Meanwhile, sexual snail populations remained much more stable over time.[25][26]
However, Hanley et al.[27] studied mite infestations of a parthenogenetic gecko species and its two related sexual ancestral species. Contrary to expectation based on the Red Queen hypothesis, they found that the prevalence, abundance and mean intensity of mites in sexual geckos was significantly higher than in asexuals sharing the same habitat.
In 2011, researchers used the microscopic roundworm Caenorhabditis elegans as a host and the pathogenic bacteria Serratia marcescens to generate a host-parasite coevolutionary system in a controlled environment, allowing them to conduct more than 70 evolution experiments testing the Red Queen Hypothesis. They genetically manipulated the mating system of C. elegans, causing populations to mate either sexually, by self-fertilization, or a mixture of both within the same population. Then they exposed those populations to the S. marcescens parasite. It was found that the self-fertilizing populations of C. elegans were rapidly driven extinct by the coevolving parasites while sex allowed populations to keep pace with their parasites, a result consistent with the Red Queen Hypothesis.[28][29] In natural populations of C. elegans, self-fertilization is the predominant mode of reproduction, but infrequent out-crossing events occur at a rate of about 1%.[30]
Critics of the Red Queen hypothesis question whether the constantly changing environment of hosts and parasites is sufficiently common to explain the evolution of sex. In particular, Otto and Nuismer [31] presented results showing that species interactions (e.g. host vs parasite interactions) typically select against sex. They concluded that, although the Red Queen hypothesis favors sex under certain circumstances, it alone does not account for the ubiquity of sex. Otto and Gerstein [32] further stated that "it seems doubtful to us that strong selection per gene is sufficiently commonplace for the Red Queen hypothesis to explain the ubiquity of sex". Parker[33] reviewed numerous genetic studies on plant disease resistance and failed to uncover a single example consistent with the assumptions of the Red Queen hypothesis.
Disadvantages of sex and sexual reproduction
The paradox of the existence of sexual reproduction is that though it is ubiquitous in multicellular organisms, there are ostensibly many inherent disadvantages to reproducing sexually when weighed against the relative advantages of alternative forms of reproduction, such as asexual reproduction. Thus, because sexual reproduction abounds in complex multicellular life, there must be some significant benefit(s) to sex and sexual reproduction that compensates for these fundamental disadvantages.
Population expansion cost of sex
Among the most limiting disadvantages to the evolution of sexual reproduction by natural selection is that an asexual population can grow much more rapidly than a sexual one with each generation.
For example, assume that the entire population of some theoretical species has 100 total organisms consisting of two sexes (i.e. males and females), with 50:50 male-to-female representation, and that only the females of this species can bear offspring. If all capable members of this population procreated once, a total of 50 offspring would be produced (the F1 generation). Contrast this outcome with an asexual species, in which each and every member of an equally sized 100-organism population is capable of bearing young. If all capable members of this asexual population procreated once, a total of 100 offspring would be produced – twice as many as produced by the sexual population in a single generation.
This diagram illustrates the two-fold cost of sex. If each individual were to contribute to the same number of offspring (two), (a) the sexual population remains the same size each generation, where the (b) asexual population doubles in size each generation.
This idea is sometimes referred to as the two-fold cost of sexual reproduction. It was first described mathematically by John Maynard Smith.[34][page needed] In his manuscript, Smith further speculated on the impact of an asexual mutant arising in a sexual population, which suppresses meiosis and allows eggs to develop into offspring genetically identical to the mother by mitotic division.[35][page needed] The mutant-asexual lineage would double its representation in the population each generation, all else being equal.
Technically the problem above is not one of sexual reproduction but of having a subset of organisms incapable of bearing offspring. Indeed, some multicellular organisms (isogamous) engage in sexual reproduction but all members of the species are capable of bearing offspring.[36][page needed] The two-fold reproductive disadvantage assumes that males contribute only genes to their offspring and sexual females spend half their reproductive potential on sons.[35][page needed] Thus, in this formulation, the principal cost of sex is that males and females must successfully copulate, which almost always involves expending energy to come together through time and space. Asexual organisms need not expend the energy necessary to find a mate.
Selfish cytoplasmic genes
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Sexual reproduction implies that chromosomes and alleles segregate and recombine in every generation, but not all genes are transmitted together to the offspring.[35][page needed] There is a chance of spreading mutants that cause unfair transmission at the expense of their non-mutant colleagues. These mutations are referred to as "selfish" because they promote their own spread at the cost of alternative alleles or of the host organism; they include nuclear meiotic drivers and selfish cytoplasmic genes.[35][page needed] Meiotic drivers are genes that distort meiosis to produce gametes containing themselves more than the 50% of the time expected by chance. A selfish cytoplasmic gene is a gene located in an organelle, plasmid or intracellular parasite that modifies reproduction to cause its own increase at the expense of the cell or organism that carries it.[35][page needed]
Genetic heritability cost of sex
A sexually reproducing organism only passes on ~50% of its own genetic material to each L2 offspring. This is a consequence of the fact that gametes from sexually reproducing species are haploid. Again, however, this is not applicable to all sexual organisms. There are numerous species which are sexual but do not have a genetic-loss problem because they do not produce males or females. Yeast, for example, are isogamous sexual organisms which have two mating types which fuse and recombine their haploid genomes. Both sexes reproduce during the haploid and diploid stages of their life cycle and have a 100% chance of passing their genes into their offspring.[36][page needed]
Some species avoid the 50% cost of sexual reproduction, although they have "sex" (in the sense of genetic recombination). In these species (e.g., bacteria, ciliates, dinoflagellates and diatoms), "sex" and reproduction occur separately.[37][38]
DNA repair and complementation
As discussed in the earlier part of this article, sexual reproduction is conventionally explained as an adaptation for producing genetic variation through allelic recombination. As acknowledged above, however, serious problems with this explanation have led many biologists to conclude that the benefit of sex is a major unsolved problem in evolutionary biology.
An alternative "informational" approach to this problem has led to the view that the two fundamental aspects of sex, genetic recombination and outcrossing, are adaptive responses to the two major sources of "noise" in transmitting genetic information. Genetic noise can occur as either physical damage to the genome (e.g. chemically altered bases of DNA or breaks in the chromosome) or replication errors (mutations).[39][13][14] This alternative view is referred to as the repair and complementation hypothesis, to distinguish it from the traditional variation hypothesis.
The repair and complementation hypothesis assumes that genetic recombination is fundamentally a DNA repair process, and that when it occurs during meiosis it is an adaptation for repairing the genomic DNA which is passed on to progeny. Recombinational repair is the only repair process known which can accurately remove double-strand damages in DNA, and such damages are both common in nature and ordinarily lethal if not repaired. For instance, double-strand breaks in DNA occur about 50 times per cell cycle in human cells (see naturally occurring DNA damage). Recombinational repair is prevalent from the simplest viruses to the most complex multicellular eukaryotes. It is effective against many different types of genomic damage, and in particular is highly efficient at overcoming double-strand damages. Studies of the mechanism of meiotic recombination indicate that meiosis is an adaptation for repairing DNA. [40] These considerations form the basis for the first part of the repair and complementation hypothesis.
In some lines of descent from the earliest organisms, the diploid stage of the sexual cycle, which was at first transient, became the predominant stage, because it allowed complementation — the masking of deleterious recessive mutations (i.e. hybrid vigor or heterosis). Outcrossing, the second fundamental aspect of sex, is maintained by the advantage of masking mutations and the disadvantage of inbreeding (mating with a close relative) which allows expression of recessive mutations (commonly observed as inbreeding depression). This is in accord with Charles Darwin,[41] who concluded that the adaptive advantage of sex is hybrid vigor; or as he put it, "the offspring of two individuals, especially if their progenitors have been subjected to very different conditions, have a great advantage in height, weight, constitutional vigor and fertility over the self fertilised offspring from either one of the same parents."
However, outcrossing may be abandoned in favor of parthenogenesis or selfing (which retain the advantage of meiotic recombinational repair) under conditions in which the costs of mating are very high. For instance, costs of mating are high when individuals are rare in a geographic area, such as when there has been a forest fire and the individuals entering the burned area are the initial ones to arrive. At such times mates are hard to find, and this favors parthenogenic species.
In the view of the repair and complementation hypothesis, the removal of DNA damage by recombinational repair produces a new, less deleterious form of informational noise, allelic recombination, as a by-product. This lesser informational noise generates genetic variation, viewed by some as the major effect of sex, as discussed in the earlier parts of this article.
Deleterious mutation clearance
Mutations can have many different effects upon an organism. It is generally believed that the majority of non-neutral mutations are deleterious, which means that they will cause a decrease in the organism's overall fitness.[42][page range too broad] If a mutation has a deleterious effect, it will then usually be removed from the population by the process of natural selection. Sexual reproduction is believed to be more efficient than asexual reproduction in removing those mutations from the genome.[43]
There are two main hypotheses which explain how sex may act to remove deleterious genes from the genome.
Evading harmful mutation build-up
Main article: Muller's ratchet
While DNA is able to recombine to modify alleles, DNA is also susceptible to mutations within the sequence that can affect an organism in a negative manner. Asexual organisms do not have the ability to recombine their genetic information to form new and differing alleles. Once a mutation occurs in the DNA or other genetic carrying sequence, there is no way for the mutation to be removed from the population until another mutation occurs that ultimately deletes the primary mutation. This is rare among organisms.
Hermann Joseph Muller introduced the idea that mutations build up in asexual reproducing organisms. Muller described this occurrence by comparing the mutations that accumulate as a ratchet. Each mutation that arises in asexually reproducing organisms turns the ratchet once. The ratchet is unable to be rotated backwards, only forwards. The next mutation that occurs turns the ratchet once more. Additional mutations in a population continually turn the ratchet and the mutations, mostly deleterious, continually accumulate without recombination.[44] These mutations are passed onto the next generation because the offspring are exact genetic clones of their parents. The genetic load of organisms and their populations will increase due to the addition of multiple deleterious mutations and decrease the overall reproductive success and fitness.
For sexually reproducing populations, studies have shown that single-celled bottlenecks are beneficial for resisting mutation build-up[citation needed]. Passaging a population through a single-celled bottleneck involves the fertilization event occurring with haploid sets of DNA, forming one fertilized cell. For example, humans undergo a single-celled bottleneck in that the haploid sperm fertilizes the haploid egg, forming the diploid zygote, which is unicellular. This passage through a single cell is beneficial in that it lowers the chance of mutations from being passed on through multiple individuals. Instead, the mutation is only passed onto one individual.[45] Further studies using Dictyostelium discoideum suggest that this unicellular initial stage is important for resisting mutations due to the importance of high relatedness. Highly related individuals are more closely related, and more clonal, whereas less related individuals are less so, increasing the likelihood that an individual in a population of low relatedness may have a detrimental mutation. Highly related populations also tend to thrive better than lowly related because the cost of sacrificing an individual is greatly offset by the benefit gained by its relatives and in turn, its genes, according to kin selection. The studies with D. discoideum showed that conditions of high relatedness resisted mutant individuals more effectively than those of low relatedness, suggesting the importance of high relatedness to resist mutations from proliferating.[46]
Removal of deleterious genes
Diagram illustrating different relationships between numbers of mutations and fitness. Kondrashov's model requires synergistic epistasis, which is represented by the red line[47][48] – each subsequent mutation has a disproportionately large effect on the organism's fitness.
This hypothesis was proposed by Alexey Kondrashov, and is sometimes known as the deterministic mutation hypothesis.[43] It assumes that the majority of deleterious mutations are only slightly deleterious, and affect the individual such that the introduction of each additional mutation has an increasingly large effect on the fitness of the organism. This relationship between number of mutations and fitness is known as synergistic epistasis.
By way of analogy, think of a car with several minor faults. Each is not sufficient alone to prevent the car from running, but in combination, the faults combine to prevent the car from functioning.
Similarly, an organism may be able to cope with a few defects, but the presence of many mutations could overwhelm its backup mechanisms.
Kondrashov argues that the slightly deleterious nature of mutations means that the population will tend to be composed of individuals with a small number of mutations. Sex will act to recombine these genotypes, creating some individuals with fewer deleterious mutations, and some with more. Because there is a major selective disadvantage to individuals with more mutations, these individuals die out. In essence, sex compartmentalises the deleterious mutations.
There has been much criticism of Kondrashov's theory, since it relies on two key restrictive conditions. The first requires that the rate of deleterious mutation should exceed one per genome per generation in order to provide a substantial advantage for sex. While there is some empirical evidence for it (for example in Drosophila[49] and E. coli[50]), there is also strong evidence against it. Thus, for instance, for the sexual species Saccharomyces cerevisiae (yeast) and Neurospora crassa (fungus), the mutation rate per genome per replication are 0.0027 and 0.0030 respectively. For the nematode worm Caenorhabditis elegans, the mutation rate per effective genome per sexual generation is 0.036.[51] Secondly, there should be strong interactions among loci (synergistic epistasis), a mutation-fitness relation for which there is only limited evidence.[52][53] Conversely, there is also the same amount of evidence that mutations show no epistasis (purely additive model) or antagonistic interactions (each additional mutation has a disproportionally small effect).
Other explanations
Geodakyan's evolutionary theory of sex
Geodakyan suggested that sexual dimorphism provides a partitioning of a species' phenotypes into at least two functional partitions: a female partition that secures beneficial features of the species and a male partition that emerged in species with more variable and unpredictable environments. The male partition is suggested to be an "experimental" part of the species that allows the species to expand their ecological niche, and to have alternative configurations. This theory underlines the higher variability and higher mortality in males, in comparison to females. This functional partitioning also explains the higher susceptibility to disease in males, in comparison to females and therefore includes the idea of "protection against parasites" as another functionality of male sex. Geodakyan's evolutionary theory of sex was developed in Russia in 1960–1980 and was not known to the West till the era of the Internet. Trofimova, who analysed psychological sex differences, hypothesised that the male sex might also provide a "redundancy pruning" function.[54]
Speed of evolution
Ilan Eshel suggested that sex prevents rapid evolution. He suggests that recombination breaks up favourable gene combinations more often than it creates them, and sex is maintained because it ensures selection is longer-term than in asexual populations – so the population is less affected by short-term changes.[17]: 85–86 [55] This explanation is not widely accepted, as its assumptions are very restrictive.
It has recently been shown in experiments with Chlamydomonas algae that sex can remove the speed limit[clarification needed] on evolution.[56]
An information theoretic analysis using a simplified but useful model shows that in asexual reproduction, the information gain per generation of a species is limited to 1 bit per generation, while in sexual reproduction, the information gain is bounded by
G
{\displaystyle {\sqrt {G}}}, where
G
{\displaystyle G} is the size of the genome in bits.[57]
Libertine bubble theory
The evolution of sex can alternatively be described as a kind of gene exchange that is independent from reproduction.[58] According to the Thierry Lodé's "libertine bubble theory", sex originated from an archaic gene transfer process among prebiotic bubbles.[59][60] The contact among the pre-biotic bubbles could, through simple food or parasitic reactions, promote the transfer of genetic material from one bubble to another. That interactions between two organisms be in balance appear to be a sufficient condition to make these interactions evolutionarily efficient, i.e. to select bubbles that tolerate these interactions ("libertine" bubbles) through a blind evolutionary process of self-reinforcing gene correlations and compatibility.[61]
The "libertine bubble theory" proposes that meiotic sex evolved in proto-eukaryotes to solve a problem that bacteria did not have, namely a large amount of DNA material, occurring in an archaic step of proto-cell formation and genetic exchanges. So that, rather than providing selective advantages through reproduction, sex could be thought of as a series of separate events which combines step-by-step some very weak benefits of recombination, meiosis, gametogenesis and syngamy.[62] Therefore, current sexual species could be descendants of primitive organisms that practiced more stable exchanges in the long term, while asexual species have emerged, much more recently in evolutionary history, from the conflict of interest resulting from anisogamy.[clarification needed]
Parasites and Muller's ratchet
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R. Stephen Howard and Curtis Lively were the first to suggest that the combined effects of parasitism and mutation accumulation can lead to an increased advantage to sex under conditions not otherwise predicted (Nature, 1994). Using computer simulations, they showed that when the two mechanisms act simultaneously the advantage to sex over asexual reproduction is larger than for either factor operating alone.
Origin of sexual reproduction
Life timeline
Many protists reproduce sexually, as do many multicellular plants, animals, and fungi. In the eukaryotic fossil record, sexual reproduction first appeared about 2.0 billion years ago in the Proterozoic Eon,[63][64] although a later date, 1.2 billion years ago, has also been presented.[65][66] Nonetheless, all sexually reproducing eukaryotic organisms likely derive from a single-celled common ancestor.[1][67][59] It is probable that the evolution of sex was an integral part of the evolution of the first eukaryotic cell.[68][69] There are a few species which have secondarily lost this feature, such as Bdelloidea and some parthenocarpic plants.
Diploidy
Organisms need to replicate their genetic material in an efficient and reliable manner. The necessity to repair genetic damage is one of the leading theories explaining the origin of sexual reproduction. Diploid individuals can repair a damaged section of their DNA via homologous recombination, since there are two copies of the gene in the cell and if one copy is damaged, the other copy is unlikely to be damaged at the same site.
A harmful damage in a haploid individual, on the other hand, is more likely to become fixed (i.e. permanent), since any DNA repair mechanism would have no source from which to recover the original undamaged sequence.[39] The most primitive form of sex may have been one organism with damaged DNA replicating an undamaged strand from a similar organism in order to repair itself.[70]
Meiosis
Sexual reproduction appears to have arisen very early in eukaryotic evolution, implying that the essential features of meiosis were already present in the last eukaryotic common ancestor.[71][67][72] In extant organisms, proteins with central functions in meiosis are similar to key proteins in natural transformation in bacteria and DNA transfer in archaea.[72][73] For example, recA recombinase, that catalyses the key functions of DNA homology search and strand exchange in the bacterial sexual process of transformation, has orthologs in eukaryotes that perform similar functions in meiotic recombination[72]
Natural transformation in bacteria, DNA transfer in archaea, and meiosis in eukaryotic microorganisms are induced by stressful circumstances such as overcrowding, resource depletion, and DNA damaging conditions.[61][72][73] This suggests that these sexual processes are adaptations for dealing with stress, particularly stress that causes DNA damage. In bacteria, these stresses induce an altered physiologic state, termed competence, that allows active take-up of DNA from a donor bacterium and the integration of this DNA into the recipient genome (see Natural competence) allowing recombinational repair of the recipients' damaged DNA.[74]
If environmental stresses leading to DNA damage were a persistent challenge to the survival of early microorganisms, then selection would likely have been continuous through the prokaryote to eukaryote transition,[62][72] and adaptative adjustments would have followed a course in which bacterial transformation or archaeal DNA transfer naturally gave rise to sexual reproduction in eukaryotes.
Virus-like RNA-based origin
Sex might also have been present even earlier, in the hypothesized RNA world that preceded DNA cellular life forms.[75] One proposed origin of sex in the RNA world was based on the type of sexual interaction that is known to occur in extant single-stranded segmented RNA viruses, such as influenza virus, and in extant double-stranded segmented RNA viruses such as reovirus.[76]
Exposure to conditions that cause RNA damage could have led to blockage of replication and death of these early RNA life forms. Sex would have allowed re-assortment of segments between two individuals with damaged RNA, permitting undamaged combinations of RNA segments to come together, thus allowing survival. Such a regeneration phenomenon, known as multiplicity reactivation, occurs in the influenza virus[77] and reovirus.[78]
Parasitic DNA elements
Another theory is that sexual reproduction originated from selfish parasitic genetic elements that exchange genetic material (that is: copies of their own genome) for their transmission and propagation. In some organisms, sexual reproduction has been shown to enhance the spread of parasitic genetic elements (e.g. yeast, filamentous fungi).[79]
Bacterial conjugation is a form of genetic exchange that some sources describe as "sex", but technically is not a form of reproduction, even though it is a form of horizontal gene transfer. However, it does support the "selfish gene" part theory, since the gene itself is propagated through the F-plasmid.[70]
A similar origin of sexual reproduction is proposed to have evolved in ancient haloarchaea as a combination of two independent processes: jumping genes and plasmid swapping.[80]
Partial predation
A third theory is that sex evolved as a form of cannibalism: One primitive organism ate another one, but instead of completely digesting it, some of the eaten organism's DNA was incorporated into the DNA of the eater.[70][68]
Vaccination-like process
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Sex may also be derived from another prokaryotic process. A comprehensive theory called "origin of sex as vaccination" proposes that eukaryan sex-as-syngamy (fusion sex) arose from prokaryan unilateral sex-as-infection, when infected hosts began swapping nuclearised genomes containing coevolved, vertically transmitted symbionts that provided protection against horizontal superinfection by other, more virulent symbionts.
Consequently, sex-as-meiosis (fission sex) would evolve as a host strategy for uncoupling from (and thereby render impotent) the acquired symbiotic/parasitic genes.[81]
Mechanistic origin of sexual reproduction
While theories positing fitness benefits that led to the origin of sex are often problematic,[citation needed] several theories addressing the emergence of the mechanisms of sexual reproduction have been proposed.
Viral eukaryogenesis
Main article: Viral eukaryogenesis
The viral eukaryogenesis (VE) theory proposes that eukaryotic cells arose from a combination of a lysogenic virus, an archaean, and a bacterium. This model suggests that the nucleus originated when the lysogenic virus incorporated genetic material from the archaean and the bacterium and took over the role of information storage for the amalgam. The archaeal host transferred much of its functional genome to the virus during the evolution of cytoplasm, but retained the function of gene translation and general metabolism. The bacterium transferred most of its functional genome to the virus as it transitioned into a mitochondrion.[82]
For these transformations to lead to the eukaryotic cell cycle, the VE hypothesis specifies a pox-like virus as the lysogenic virus. A pox-like virus is a likely ancestor because of its fundamental similarities with eukaryotic nuclei. These include a double stranded DNA genome, a linear chromosome with short telomeric repeats, a complex membrane bound capsid, the ability to produce capped mRNA, and the ability to export the capped mRNA across the viral membrane into the cytoplasm. The presence of a lysogenic pox-like virus ancestor explains the development of meiotic division, an essential component of sexual reproduction.[83]
Meiotic division in the VE hypothesis arose because of the evolutionary pressures placed on the lysogenic virus as a result of its inability to enter into the lytic cycle. This selective pressure resulted in the development of processes allowing the viruses to spread horizontally throughout the population. The outcome of this selection was cell-to-cell fusion. (This is distinct from the conjugation methods used by bacterial plasmids under evolutionary pressure, with important consequences.)[82] The possibility of this kind of fusion is supported by the presence of fusion proteins in the envelopes of the pox viruses that allow them to fuse with host membranes. These proteins could have been transferred to the cell membrane during viral reproduction, enabling cell-to-cell fusion between the virus host and an uninfected cell. The theory proposes meiosis originated from the fusion between two cells infected with related but different viruses which recognised each other as uninfected. After the fusion of the two cells, incompatibilities between the two viruses result in a meiotic-like cell division.[83]
The two viruses established in the cell would initiate replication in response to signals from the host cell. A mitosis-like cell cycle would proceed until the viral membranes dissolved, at which point linear chromosomes would be bound together with centromeres. The homologous nature of the two viral centromeres would incite the grouping of both sets into tetrads. It is speculated that this grouping may be the origin of crossing over, characteristic of the first division in modern meiosis. The partitioning apparatus of the mitotic-like cell cycle the cells used to replicate independently would then pull each set of chromosomes to one side of the cell, still bound by centromeres. These centromeres would prevent their replication in subsequent division, resulting in four daughter cells with one copy of one of the two original pox-like viruses. The process resulting from combination of two similar pox viruses within the same host closely mimics meiosis.[83]
Neomuran revolution
An alternative theory, proposed by Thomas Cavalier-Smith, was labeled the Neomuran revolution. The designation "Neomuran revolution" refers to the appearances of the common ancestors of eukaryotes and archaea. Cavalier-Smith proposes that the first neomurans emerged 850 million years ago. Other molecular biologists assume that this group appeared much earlier, but Cavalier-Smith dismisses these claims because they are based on the "theoretically and empirically" unsound model of molecular clocks. Cavalier-Smith's theory of the Neomuran revolution has implications for the evolutionary history of the cellular machinery for recombination and sex. It suggests that this machinery evolved in two distinct bouts separated by a long period of stasis; first the appearance of recombination machinery in a bacterial ancestor which was maintained for 3 Gy(billion years), until the neomuran revolution when the mechanics were adapted to the presence of nucleosomes. The archaeal products of the revolution maintained recombination machinery that was essentially bacterial, whereas the eukaryotic products broke with this bacterial continuity. They introduced cell fusion and ploidy cycles into cell life histories. Cavalier-Smith argues that both bouts of mechanical evolution were motivated by similar selective forces: the need for accurate DNA replication without loss of viability.[84]
Questions
Some questions biologists have attempted to answer include:
Why does sexual reproduction exist, if in many organisms it has a 50% cost (fitness disadvantage) in relation to asexual reproduction?[37]
Did mating types (types of gametes, according to their compatibility) arise as a result of anisogamy (gamete dimorphism), or did mating types evolve before anisogamy?[85][86]
Why do most sexual organisms use a binary mating system? Grouping itself offers a survival advantage. A binary recognition based system is the most simple and effective method in maintaining species grouping.[87]
Why do some organisms have gamete dimorphism?
References
Letunic, I; Bork, P (2006). "Interactive Tree of Life". Retrieved 23 July 2011.
mLetunic, I; Bork, P (2007). "Interactive Tree of Life (iTOL): An online tool for phylogenetic tree display and annotation" (PDF). Bioinformatics. 23 (1): 127–8. doi:10.1093/bioinformatics/btl529. PMID 17050570.
Letunic, I; Bork, P (2011). "Interactive Tree of Life v2: Online annotation and display of phylogenetic trees made easy" (PDF). Nucleic Acids Research. 39 (Web Server issue): W475–8. doi:10.1093/nar/gkr201. PMC 3125724. PMID 21470960.
Otto, Sarah (2014). "Sexual Reproduction and the Evolution of Sex". Scitable. Retrieved 28 February 2019.
Redfield, Rosemary J. (August 2001). "Do bacteria have sex?". Nature Reviews Genetics. 2 (8): 634–639. doi:10.1038/35084593. PMID 11483988. S2CID 5465846.
Goodenough, U.; Heitman, J. (1 March 2014). "Origins of Eukaryotic Sexual Reproduction". Cold Spring Harbor Perspectives in Biology. 6 (3): a016154. doi:10.1101/cshperspect.a016154. ISSN 1943-0264. PMC 3949356. PMID 24591519.
Darwin, Erasmus (1800). Phytologia …. Dublin, Ireland: P. Byrne. p. 104. From p. 104: "As the progeny by lateral generation [i.e., vegetative (asexual) reproduction] so exactly resembles the parent stock, it follows, that though any new variety, or improvement, may be thus continued for a century or two, as in grafted fruit-trees, yet that no new variety or improvements can be obtained by this mode of generation; … " "But from the sexual, or amatorial, generation of plants new varieties, or improvements, are frequently obtained; as many of the young plants from seeds are dissimilar to the parent, and some of them supererior to the parent in the qualities we wish to possess; … " " … another advantage occurs from sexual generation, which is the production of new species of plants, or mules, … "
English translation: Weismann, August (1889). Poulton, Edward B.; Schönland, Selmar; Shipley, Arthur E. (eds.). Essays Upon Heredity and Kindred Biological Problems. Oxford, England: Clarendon Press. pp. 252–332. Ch. 5: The Significance of Sexual Reproduction in the Theory of Natural Selection (1886)
Weismann, Aug. (1885) "Die Bedeutung der sexuellen Fortpflanzung für die Selektions-Theorie" [The significance of sexual reproduction in the theory of natural selection] Stilling, J. (ed.) Tageblatt der 58. Versammlung Deutscher Naturforscher und Aerzte in Strassburg [Daily News of the 58th Conference of German Natural Scientists and Physicians in Strassburg] (in German) Strassburg, Germany: G. Fischbach pp. 42-56.
Revised and expanded in: Weismann, August (1886). Die Bedeutung der sexuellen Fortpflanzung für die Selektions-Theorie (in German). Jena, Germany: Gustav Fischer.
Darwin, Charles (1876). The Effects of Cross and Self Fertilisation in the Vegetable Kingdom. London, England: John Murray. p. 462.
Crow J.F. (1994). Advantages of Sexual Reproduction, Dev. Gen., vol.15, pp. 205-213.
Goldstein, R N (2010). 36 Arguments for the Existence of God: A Work of Fiction. Pantheon. ISBN 978-0-307-37818-7.
Baer, C. F. (2008). "NCBI". PLOS Biology. 6 (2): e52. doi:10.1371/journal.pbio.0060052. PMC 2253642. PMID 18303954.
Bernstein H, Byerly HC, Hopf FA, Michod RE (September 1985). "Genetic damage, mutation, and the evolution of sex". Science. 229 (4719): 1277–81 doi:10.1126/science.3898363. PMID 3898363
Bernstein H, Hopf FA, Michod RE (1987). "The molecular basis of the evolution of sex". Adv Genet. 24: 323–70. doi:10.1016/s0065-2660(08)60012-7. PMID 3324702
Heng HH; Heng, Henry H.Q. (2007). "Elimination of altered karyotypes by sexual reproduction preserves species identity". Genome. 50 (5): 517–524. doi:10.1139/g07-039. PMID 17612621.
Gorelick R, Heng HH; Heng (2011). "Sex reduces genetic variation: a multidisciplinary review". Evolution. 65 (4): 1088–1098. doi:10.1111/j.1558-5646.2010.01173.x. PMID 21091466. S2CID 7714974.
Birdsell, JA; Wills, C (2003). "The Evolutionary Origin and Maintenance of Sexual Recombination: A Review of Contemporary Models". Evolutionary Biology. Vol. 33. pp. 27–137. doi:10.1007/978-1-4757-5190-1_2. ISBN 978-1-4419-3385-0.
Gorelick R, Viillablanca, FX. Meiosis decreases recombination load: Mitosis increases recombination load. Ideas in Ecology and Evolution 11:19-28, 2018 doi:10.4033/iee.2018.11.3.n
Matt Ridley 1995 The Red Queen: Sex and the Evolution of Human Nature 1995 Penguin.
MacIntyre, Ross J.; Clegg, Michael, T (Eds.), Springer. Hardcover ISBN 978-0306472619, ISBN 0306472619 Softcover ISBN 978-1-4419-3385-0.
Van Valen, L. (1973). "A New Evolutionary Law". Evolutionary Theory. 1: 1–30.
Hamilton, W. D.; Axelrod, R.; Tanese, R. (1990). "Sexual reproduction as an adaptation to resist parasites". Proceedings of the National Academy of Sciences. 87 (9): 3566–3573. Bibcode:1990PNAS...87.3566H. doi:10.1073/pnas.87.9.3566. PMC 53943. PMID 2185476.
Kuma, K.; Iwabe, N.; Miyata, T. (1995). "Functional constraints against variations on molecules from the tissue-level - slowly evolving brain-specific genes demonstrated by protein-kinase and immunoglobulin supergene families". Molecular Biology and Evolution. 12 (1): 123–130. doi:10.1093/oxfordjournals.molbev.a040181. PMID 7877487.
Wolfe KH, Sharp PM; Sharp (1993). "Mammalian gene evolution - nucleotide-sequence divergence between mouse and rat". Journal of Molecular Evolution. 37 (4): 441–456. Bibcode:1993JMolE..37..441W. doi:10.1007/BF00178874. PMID 8308912. S2CID 10437152.
Jokela, Jukka; Dybdahl, Mark; Lively, Curtis (2009). "The Maintenance of Sex, Clonal Dynamics, and Host-Parasite Coevolution in a Mixed Population of Sexual and Asexual Snails". The American Naturalist. 174 (s1): S43–53. doi:10.1086/599080. JSTOR 10.1086/599080. PMID 19441961. S2CID 6797643.
"Parasites May Have Had Role In Evolution Of Sex". Science Daily. 31 July 2009. Retrieved 19 September 2011.
Hanley KA; Fisher RN; Case TJ (1995). "Lower mite infestations in an asexual gecko compared with its sexual ancestors". Evolution. 49 (3): 418–426. doi:10.2307/2410266. JSTOR 2410266. PMID 28565091.
Morran, Levi T.; Schmidt, Olivia G.; Gelarden, Ian A.; Parrish Rc, Raymond C.; Lively, Curtis M. (2011). "Running with the Red Queen: Host-Parasite Coevolution Selects for Biparental Sex". Science. 333 (6039): 216–218. Bibcode:2011Sci...333..216M. doi:10.1126/science.1206360. PMC 3402160. PMID 21737739.
"Sex -- As We Know It -- Works Thanks to Ever-Evolving Host-Parasite Relationships, Biologists Find". Science Daily. 9 July 2011. Retrieved 19 September 2011.
Barrière A, Félix MA (July 2005). "High local genetic diversity and low outcrossing rate in Caenorhabditis elegans natural populations". Curr. Biol. 15 (13): 1176–84. arXiv:q-bio/0508003. Bibcode:2005CBio...15.1176B. doi:10.1016/j.cub.2005.06.022. PMID 16005289. S2CID 2229622.
Otto SP, Nuismer SL; Nuismer (2004). "Species interactions and the evolution of sex". Science. 304 (5673): 1018–1020. Bibcode:2004Sci...304.1018O. doi:10.1126/science.1094072. PMID 15143283. S2CID 8599387.
Otto SP, Gerstein AC; Gerstein (August 2006). "Why have sex? The population genetics of sex and recombination". Biochemical Society Transactions. 34 (Pt 4): 519–22. doi:10.1042/BST0340519. PMID 16856849.
Parker MA (1994). "Pathogens and sex in plants". Evolutionary Ecology. 8 (5): 560–584. Bibcode:1994EvEco...8..560P. doi:10.1007/BF01238258. S2CID 31756267.
Smith, J. Maynard (1978). The Evolution of Sex. Cambridge University Press. ISBN 9780521293020.
Stearns, S. C. (2005). Evolution : an introduction. Hoekstra, Rolf F. (2nd ed.). Oxford [England]: Oxford University Press. ISBN 978-0199255634. OCLC 56964580.
Hoekstra, Rolf F. (1987). "The Evolution of Sexes". In Stearns, Stephen C. (ed.). The Evolution of Sex and its Consequences. Springer Basel AG. ISBN 9783034862738.
Ridley, Mark (2003). Evolution (3rd ed.). Wiley. p. 314. ISBN 9781405103459.
Beukeboom, L. & Perrin, N. (2014). The Evolution of Sex Determination. Oxford University Press, p. 5–6 [1]. Online resources, [2].
Bernstein H; Byerly HC; Hopf FA; Michod RE (1984). "Origin of sex". J. Theor. Biol. 110 (3): 323–51. Bibcode:1984JThBi.110..323B. doi:10.1016/S0022-5193(84)80178-2. PMID 6209512.
Cox MM (2001). "Historical overview: searching for replication help in all of the rec places". Proc. Natl. Acad. Sci. U.S.A. 98 (15): 8173–80. Bibcode:2001PNAS...98.8173C. doi:10.1073/pnas.131004998. PMC 37418. PMID 11459950.
Darwin CR (1876). The effects of cross and self fertilisation in the vegetable kingdom. London: John Murray. [3] Archived 19 February 2016 at the Wayback Machine see page 462
Griffiths et al. 1999. Gene mutations, p197-234, in Modern Genetic Analysis, New York, W.H. Freeman and Company.
Kondrashov, A. S. (1988). "Deleterious mutations and the evolution of sexual reproduction". Nature. 336 (6198): 435–440. Bibcode:1988Natur.336..435K. doi:10.1038/336435a0. PMID 3057385. S2CID 4233528.
Muller, H.J. (1964). "The Relation of Recombination to Mutational Advance". Mutation Research. 1 (1): 2–9. Bibcode:1964MRFMM...1....2M. doi:10.1016/0027-5107(64)90047-8. PMID 14195748.
Niklas, Karl J. (1 January 2014). "The evolutionary-developmental origins of multicellularity". American Journal of Botany. 101 (1): 6–25. doi:10.3732/ajb.1300314. ISSN 0002-9122. PMID 24363320.
Kuzdzal-Fick, Jennie J.; Fox, Sara A.; Strassmann, Joan E.; Queller, David C. (16 December 2011). "High Relatedness Is Necessary and Sufficient to Maintain Multicellularity in Dictyostelium". Science. 334 (6062): 1548–1551. Bibcode:2011Sci...334.1548K. doi:10.1126/science.1213272. ISSN 0036-8075. PMID 22174251. S2CID 206537272.
Ridley M (2004) Evolution, 3rd edition. Blackwell Publishing.
Charlesworth B, Charlesworth D (2010) Elements of Evolutionary Genetics. Roberts and Company Publishers.
Whitlock, M. C.; Bourguet, D. (2000). "Factors affecting the genetic load in Drosophila: synergistic epistasis and correlations among fitness components" (PDF). Evolution. 54 (5): 1654–1660. doi:10.1554/0014-3820(2000)054[1654:fatgli]2.0.co;2. PMID 11108592. S2CID 198153635.
Elena, S. F.; Lenski, R. E. (1997). "Test of synergistic interactions among deleterious mutations in bacteria". Nature. 390 (6658): 395–398. Bibcode:1997Natur.390..395E. doi:10.1038/37108. PMID 9389477. S2CID 205025450.
Drake JW; Charlesworth B; Charlesworth D; Crow JF (April 1998). "Rates of spontaneous mutation". Genetics. 148 (4): 1667–86. doi:10.1093/genetics/148.4.1667. PMC 1460098. PMID 9560386.
Sohail, M; Vakhrusheva, OA; Sul, JH; Pulit, SL; Francioli, LC; van den Berg, LH; Veldink, JH; de Bakker, PIW; Bazykin, GA; Kondrashov, AS; Sunyaev, SR (2017). "Negative selection in humans and fruit flies involves synergistic epistasis". Science. 356 (6337): 539–542. Bibcode:2017Sci...356..539S. doi:10.1126/science.aah5238. PMC 6200135. PMID 28473589.
Matheson, Joseph; Masel, Joanna (2 March 2024). "Background Selection From Unlinked Sites Causes Nonindependent Evolution of Deleterious Mutations". Genome Biology and Evolution. 16 (3): evae050. doi:10.1093/gbe/evae050. ISSN 1759-6653. PMC 10972689. PMID 38482769.
Trofimova, I. (2015). "Do psychological sex differences reflect evolutionary bi-sexual partitioning?". American Journal of Psychology. 128 (4): 485–514. doi:10.5406/amerjpsyc.128.4.0485. PMID 26721176.
Eshel, I.; Feldman, MW (May 1970). "On the evolutionary effect of recombination". Theoretical Population Biology. 1 (1): 88–100. Bibcode:1970TPBio...1...88E. doi:10.1016/0040-5809(70)90043-2. PMID 5527627.
Colegrave, N. (2002). "Sex releases the speed limit on evolution". Nature. 420 (6916): 664–666. Bibcode:2002Natur.420..664C. doi:10.1038/nature01191. hdl:1842/692. PMID 12478292. S2CID 4382757.
David MacKay (2003). Information Theory, Inference, and Learning Algorithms (PDF). Cambridge: Cambridge University Press. pp. 269–280.
Lesbarrères D (2011). "Sex or no sex, reproduction is not the question". BioEssays. 33 (11): 818. doi:10.1002/bies.201100105. PMID 22009640. S2CID 46112804.
Lodé, T (2011). "Sex is not a solution for reproduction: the libertine bubble theory". BioEssays. 33 (6): 419–422. doi:10.1002/bies.201000125. PMID 21472739.
Lodé, T (2011). "The origin of sex was interaction, not reproduction (what's sex really all about), Big Idea". New Scientist. 212 (2837): 30–31. doi:10.1016/S0262-4079(11)62719-X.
Lodé, T (2012). "Sex and the origin of genetic exchanges". Trends Evol Biol. 4: e1. doi:10.4081/eb.2012.e1.
Lodé, T (2012). "Have sex or not ? Lessons from bacteria". Sexual Dev. 6 (6): 325–328. doi:10.1159/000342879. PMID 22986519.
Otto, Sarah P. (2008). "Sexual Reproduction and the Evolution of Sex". Nature. Retrieved 1 October 2021.
Zimmer, Carl (5 June 2009). "On The Origin Of Sexual Reproduction". Science. 324 (5932): 1254–1256. doi:10.1126/science.324_1254. PMID 19498143. S2CID 39987391. Retrieved 1 October 2021.
Butterfield, Nicholas J. (2000). "Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes". Paleobiology. 26 (3): 386. Bibcode:2000Pbio...26..386B. doi:10.1666/0094-8373(2000)026<0386:BPNGNS>2.0.CO;2. S2CID 36648568. Retrieved 12 April 2021.
Cumming, Vivian (4 July 2016). "The Real Reasons Why We Have Sex". BBC News. Retrieved 12 April 2021.
Bernstein H, Bernstein C (2010). "Evolutionary origin of recombination during meiosis". BioScience. 60 (7): 498–505. doi:10.1525/bio.2010.60.7.5. S2CID 86663600.
Ploompuu, T. (1999). Biosüsteemide mälu teooria [Why the eukaryotic cell memory was needed] (in Estonian). Vol. XXV. Tartu: Sulemees. pp. 51–56. ISBN 978-9985908150. {{cite book}}: |journal= ignored (help) Abstract in English available online: [4]
Hörandl E, Speijer D (February 2018). "How oxygen gave rise to eukaryotic sex". Proc. Biol. Sci. 285 (1872): 20172706. doi:10.1098/rspb.2017.2706. PMC 5829205. PMID 29436502.
Olivia Judson (2002). Dr. Tatiana's sex advice to all creation. New York: Metropolitan Books. pp. 233–4. ISBN 978-0-8050-6331-8.
Dacks J, Roger AJ (June 1999). "The first sexual lineage and the relevance of facultative sex". Journal of Molecular Evolution. 48 (6): 779–783. Bibcode:1999JMolE..48..779D. doi:10.1007/PL00013156. PMID 10229582. S2CID 9441768.
Bernstein, H., Bernstein, C. Evolutionary origin and adaptive function of meiosis. In "Meiosis", Intech Publ (Carol Bernstein and Harris Bernstein editors), Chapter 3: 41-75 (2013).
Bernstein, H (2017). "Sexual communication in archaea, the precursor to meiosis". In Witzany, Guenther (ed.). Biocommunication of Archaea. pp. 103–117. doi:10.1007/978-3-319-65536-9. ISBN 978-3-319-65535-2. S2CID 26593032.
Michod RE, Wojciechowski MF, Hoelzer MA (1988). "DNA repair and the evolution of transformation in the bacterium Bacillus subtilis". Genetics. 118 (1): 31–39. doi:10.1093/genetics/118.1.31. PMC 1203263. PMID 8608929.
Eigen M, Gardiner W, Schuster P, Winkler-Oswatitsch R (April 1981). "The origin of genetic information". Scientific American. 244 (4): 88–92, 96, et passim. Bibcode:1981SciAm.244d..88E. doi:10.1038/scientificamerican0481-88. PMID 6164094.
Bernstein H, Byerly HC, Hopf FA, Michod RE (October 1984). "Origin of sex". Journal of Theoretical Biology. 110 (3): 323–351. Bibcode:1984JThBi.110..323B. doi:10.1016/S0022-5193(84)80178-2. PMID 6209512.
Barry RD (1961). "The multiplication of influenza virus. II. Multiplicity reactivation of ultraviolet irradiated virus". Virology. 14 (4): 398–405. doi:10.1016/0042-6822(61)90330-0. hdl:1885/109240. PMID 13687359.
McClain ME, Spendlove RS (1966). "Multiplicity reactivation of reovirus particles after exposure to ultraviolet light". J Bacteriol. 92 (5): 1422–1429. doi:10.1128/JB.92.5.1422-1429.1966. PMC 276440. PMID 5924273.
Hickey D (1982). "Selfish DNA: a sexually-transmitted nuclear parasite". Genetics. 101 (3–4): 519–531. doi:10.1093/genetics/101.3-4.519. PMC 1201875. PMID 6293914.
DasSarma, Shiladitya (2007). "Extreme Microbes". American Scientist. 95 (3): 224–231. doi:10.1511/2007.65.224.
Sterrer W (2002). "On the origin of sex as vaccination". Journal of Theoretical Biology. 216 (4): 387–396. Bibcode:2002JThBi.216..387S. doi:10.1006/jtbi.2002.3008. PMID 12151256.
Bell, PJ (2001). "Viral eukaryogenesis: Was the ancestor of the nucleus a complex DNA virus?". Journal of Molecular Biology. 53 (3): 251–256. Bibcode:2001JMolE..53..251L. doi:10.1007/s002390010215. PMID 11523012. S2CID 20542871.
Bell, PJ (2006). "Sex and the eukaryotic cell cycle is consistent with a viral ancestry for the eukaryotic nucleus". Journal of Theoretical Biology. 243 (1): 54–63. Bibcode:2006JThBi.243...54B. doi:10.1016/j.jtbi.2006.05.015. PMID 16846615.
Cavalier-Smith, Thomas (2006). "Cell evolution and Earth history: Stasis and revolution". Philosophical Transactions of the Royal Society B: Biological Sciences. 361 (1470): 969–1006. doi:10.1098/rstb.2006.1842. PMC 1578732. PMID 16754610.
T. Togashi, P. Cox (Eds.) The Evolution of Anisogamy. Cambridge University Press, Cambridge; 2011, p. 22-29.
Beukeboom, L. & Perrin, N. (2014). The Evolution of Sex Determination. Oxford University Press, p. 25 [5]. Online resources, [6].
Czárán, T.L.; Hoekstra, R.F. (2006). "Evolution of sexual asymmetry". BMC Evolutionary Biology. 4: 34–46. doi:10.1186/1471-2148-4-34. PMC 524165. PMID 15383154.
Further reading
Bell, Graham (1982). The masterpiece of nature: the evolution and genetics of sexuality. Berkeley: University of California Press. ISBN 978-0-520-04583-5.
Bernstein, Carol; Harris Bernstein (1991). Aging, sex, and DNA repair. Boston: Academic Press. ISBN 978-0-12-092860-6.
Hurst, L.D.; J.R. Peck (1996). "Recent advances in the understanding of the evolution and maintenance of sex". Trends in Ecology and Evolution. 11 (2): 46–52. Bibcode:1996TEcoE..11...46H. doi:10.1016/0169-5347(96)81041-X. PMID 21237760.
Levin, Bruce R.; Richard E. Michod (1988). The Evolution of sex: an examination of current ideas. Sunderland, Mass: Sinauer Associates. ISBN 978-0-87893-459-1.
Maynard Smith, John (1978). The evolution of sex. Cambridge, UK: Cambridge University Press. ISBN 978-0-521-21887-0.
Michod, Richard E. (1995). Eros and evolution: a natural philosophy of sex. Reading, Mass: Addison-Wesley Pub. Co. ISBN 978-0-201-40754-9.
"Scientists put sex origin mystery to bed, Wild strawberry research provides evidence on when gender emerges". NBC News. Archived from the original on 19 December 2015. Retrieved 25 November 2008.
Ridley, Mark (1993). Evolution. Oxford: Blackwell Scientific. ISBN 978-0-632-03481-9.
Ridley, Mark (2000). Mendel's demon: gene justice and the complexity of life. London: Weidenfeld & Nicolson. ISBN 978-0-297-64634-1.
Ridley, Matt (1995). The Red Queen: sex and the evolution of human nature. New York: Penguin Books. ISBN 978-0-14-024548-6.
Szathmáry, Eörs; John Maynard Smith (1995). The Major Transitions in Evolution. Oxford: W.H. Freeman Spektrum. ISBN 978-0-7167-4525-9.
Taylor, Timothy (1996). The prehistory of sex: four million years of human sexual culture. New York: Bantam Books. ISBN 978-0-553-09694-1.
Williams, George (1975). Sex and evolution. Princeton, N.J: Princeton University Press. ISBN 978-0-691-08147-2.