Misconceptions about mitochondria and mammalian fertilization: Implications for theories on human evolution

Abstract

In vertebrates, inheritance of mitochondria is thought to be predominantly maternal, and mitochondrial DNA analysis has become a standard taxonomic tool. In accordance with the prevailing view of strict maternal inheritance, many sources assert that during fertilization, the sperm tail, with its mitochondria, gets excluded from the embryo. This is incorrect. In the majority of mammalsincluding humans-the midpiece mitochondria can be identified in the embryo even though their ultimate fate is unknown. The ''missing mitochondria'' story seems to have survived-and proliferated-unchallenged in a time of contention between hypotheses of human origins, because it supports the ''African Eve'' model of recent radiation of Homo sapiens out of Africa. We will discuss the infiltration of this mistake into concepts of mitochondrial inheritance and human evolution.

Sperm Mitochondrial DNA Elimination in the Zygote of the Oogamous Brown Alga Undaria pinnatifida (Laminariales, Phaeophyceae)

“…Selective elimination of organelles (especially organellar DNA) occurs at different stages of sexual reproduction, i.e., gametogenesis, fertilization, and postfertilization (zygote development) (Birky 1995(Birky , 2001). In animals (oogamy), sperm mitochondria and mtDNA are selectively digested in the fertilized egg (Kaneda et al 1995, Ankel-Simons andCummins 1996). Uniparental inheritance of land plants is caused by organellar DNA digestion during spermatogenesis before fertilization (Nagata et al 1999).…”

Paternal products and by–products in Drosophila development

“…Other persistent paternal products include microtubular fragments of mouse sperm axonemes (Simerly et al 1993) and the sperm midpiece mitochondria of humans (Ankel-Simons & Cummins 1996), both of which are detectable up to the 32-cell morula stage, as well as the large mitochondrial derivatives of insect sperm, which have been traced to the blastoderm stage (Perotti 1973(Perotti , 1975FriedlÌnder 1980). Evidence that extragenomic, sperm-derived products are essential for development come from two sources: (1) strict paternal-e¡ect mutations resulting in embryonic lethality in Drosophila melanogaster (pal;Baker 1975) and ms(3)K81 (Fuyama 1984(Fuyama , 1986aYasuda et al 1995) and in Caenorhabditis elegans (spe-11;Browning & Strome 1996); and (2) the male sterility produced in certain intrastrain crosses by the endocellular microbe, Wolbachia (Karr 1994;Werren et al 1995).…”

Do mitochondria recombine in humans?

“…Although it has been known for over 100 years (Lillie 1923) that paternal mitochondria enter the egg in both humans (Ankel-Simons & Cummins 1996) and mice (Gyllensten et al 1991;Kaneda et al 1995;Shitara et al 1998), several textbooks and papers have stated that the mid-piece and tail of the sperm, containing all the paternal mitochondria, fall o¡ outside the egg (see Ankel-Simons & Cummins 1996). There has been, and continues to be, overwhelming evidence that this is not so.…”

“…(a) Paternal leakage Ankel-Simons & Cummins (1996) have laid the blame for evolutionary biology's belief in the clonality of mitochondria on the perpetuation of a myth, that paternal mitochondria do not enter the egg. Although it has been known for over 100 years (Lillie 1923) that paternal mitochondria enter the egg in both humans (Ankel-Simons & Cummins 1996) and mice (Gyllensten et al 1991;Kaneda et al 1995;Shitara et al 1998), several textbooks and papers have stated that the mid-piece and tail of the sperm, containing all the paternal mitochondria, fall o¡ outside the egg (see Ankel-Simons & Cummins 1996).…”