Worm sperm

You may have never thought about what feature distinguishes males from females. After all, in mammals the differences are often clear to us. In other groups too, the differences between male and female traits are often conspicuous. But, there are many species where male and female reproductive organs are both present in the same individual. Even in these species we can tell male parts from female parts.

To distinguish male from female we look at the relative size of the sex cells or gametes. Males produce the smaller gametes (e.g. sperm) and females produce the larger gametes (e.g. eggs). This difference in the size of the gametes is known as anisogamy, which essentially means without ("an") the same ("iso") gametes ("gamy"). 

The converse of anisogamy is isogamy. Species that are isogamous are very rare now, but this is thought to be the ancestral condition. As in anisogamous species where fertilisation only occurs when egg and sperm meet, fertilisation cannot occur in isogamous species unless the gametes of two different mating types meet. In isogamous species mating types are are referred to by various names, such as "+" and "-", in place of male and female.

The origins of anisogamy are unclear, but we have a pretty good explanation for why it evolved. Each gamete an individual produces costs energy and it must be stocked with additional reserves so that the zygote can complete development and start acquiring it's own energy. In isogamy, each member of a pair contributes half the energy to produce a viable offspring. In anisogamy, the cost is overwhelmingly paid by one of the mating types.

Investing almost nothing in individual gametes comes with a huge advantage, vastly more gametes can be produced increasing the number of offspring you can potentially produce. The more gametes an individual has the more fertilisations and individual can potentially achieve. Once one mating type gets far enough down the path of small gametes, its pair can't follow because that is likely to result in a zygote that doesn't have enough resources to survive.

It is relatively clear that fertilisation success has driven the evolution of males that produce more, small sperm. However, there are other aspects of sperm size and shape that appear to contribute to fertilisation success and these are surprisingly variable among and within species. Clear demonstrations that differences in sperm characteristics affect fertilisation success are rare, which makes a new paper in Evolution particularly interesting. 

Darren Johnson of the National Centre for Ecological Analysis and Synthesis, with Keyne Monro and Dustin Marshall of UQ (now both at Monash) looked at sperm traits in the broadcast spawning tubeworm, Galeolaria gemineoa. These worms can occur individually or in huge aggregations, leading to substantial variation in the concentrations of sperm and eggs in the wild. Because they don't leave their tubes, their options for increasing fertilisation success are limited relative to mobile species.

A colony of Galeolaria caespitosa, which are nearly identical to G. gemineoa (photo D. Semmens).

Groups of eggs from multiple females were exposed to the sperm of a single male at six different concentrations and two different ages. Fertilisation success was measured at the proportion of eggs that were undergoing normal development within each treatment. This is not a direct measure of fertilisation success because some embryos may have died very early due to genetic incompatibilities rather than the absence of fertilisation. However, it is a reasonable and practical proxy.

At high sperm concentrations, males that produced sperm with longer average tail length and smaller average head size achieved greater fertilisation success. In contrast, males that produced sperm with longer than average heads were favored at low sperm concentrations and older age. The results suggest that variation in sperm size and shape within a species may be preserved because different fertilisation environments favor contrasting sperm characteristics. 

The logistics of genetically assigning paternity prevented the authors from varying sperm competition environments. Had the sperm of multiple males been in competition to fertilise the eggs, different traits or trait combinations could have been favoured. While it is probably more realistic to pit the sperm of several males against each other, single male experiments still provide useful insights into selection on sperm traits.

An abbreviated version of this post also appears in the Research Highlights on the Australasian Evolution Society website.

References:

Johnson, D., Monro, K., & Marshall, D. (2013). The maintenance of sperm variability: Context-dependent selection on sperm morphology in a broadcast spawning invertebrate Evolution, 67 (5), 1383-1395 DOI: 10.1111/evo.12022

Alvin

The Deep Submergence Vehicle Alvin is the best known marine research vessel. It was commissioned by the United States Navy in 1964, but it calls Woods Hole Oceanographic Institution home. For its 49th birthday, it's received a refit that will increase its dive range by two kilometers and give the people inside more room and greater vision. Unfortunately, due to the limitations of its batteries, Alvin won't be able to reach its rated depth for another few years. Lithium-ion batteries are considered to be too great a fire risk at the moment.

Alvin returning to the surface carrying samples (photo Wikipedia)

Alvin sprang to fame in 1977 when scientists inside it made the first observations of hydrothermal vent communities off the Galapagos Islands. These were the first communities of multicellular organisms ever discovered that were able to survive in isolation from the sun. To marine biologists, the discovery of hydrothermal vent communities was more exciting than the moon landings less than a decade earlier. And it was Alvin, like Apollo 11, that made it possible. Unlike Apollo 11, Alvin continues to make discoveries and has contributed more to marine science than any other vehicle.

Living fossils are evolving

Charles Darwin coined the term living fossil in On the Origin of Species. He didn’t use it the same way that it has come to be used. He suggested that living fossils are modern species that can be used to link to groups in the same way that fossils can. One of the examples he gave was the platypus, which lactates and lays eggs, which is evidence that mammals and reptiles share a common ancestor. I don't think he meant it to mean an unchanged relict, as some people interpret his words.

Today, a living fossil is a species that retains many features of their fossil ancestor so that it is recognisably closely related. There are some stunning examples of this, such as orb-weaving spiders. In 2011 a 165 million year old spider fossil was described by Seldon et al., which shared so many features with modern Nephila spiders that it was placed within the same genus. Interestingly, I have never heard of web building spiders being referred to as living fossils despite there being amazing conservation of traits in many groups.

The orb-weaving spiders Nephila clavipes (left) and N. jurassica (right) are separated by 165 million years, but placed within the same genus (image of N. clavipes from Wikipedia and N. jurassica from Seldon et al. 2011).

Unfortunately, living fossil has become synonymous with a species, or group of species, displaying no evolutionary change or very slow change. This is completely wrong. Although the conservation of morphology in Nephila is remarkable, there are more than 150 known species in the genus. Clearly there has been evolutionary diversification within the group. Indeed, whenever living fossils are examined in more than superficial detail it becomes difficult to see them as organisms that evolution forgot.

Horseshoe crabs are one of the most iconic living fossils. There are four living species in three genera. They are placed within the subphylum chelicerata, which makes them more closely related to spiders and scorpions than they are to true crabs, which are placed within the subphylum crustacea. Although there are fewer species of horseshoe crabs than Nephila, that fact that there are four species that are all different from fossil species is a strong indication that evolution hasn't stopped for them.

The Atlantic horseshoe crab, Limulus polyphemus, mating (photo Wikipedia)

The general shape of modern horseshoe crabs is strikingly similar to the fossils that date from about 450 million years ago. Close examination, though, shows that parts of their shape, their legs in particular, have changed over time. Briggs et al. 2012 looked at a fossil horseshoe crab from 425 million years ago, which is relatively early in their evolution. They found that modern horseshoe crabs are missing an entire set of limbs that were present in their ancestors.

All modern chelicerates, including living horseshoe crabs, have unbranched limbs; each limb is a single series of segments. Most crustaceans have limbs that branch at the base into two series of segments. Branched limbs, like those in crustaceans, are the ancestral condition and unbranched limbs are thought to have evolved several times among the arthropods. Indeed, Briggs et al. found that the fossil horseshoe crab had branched limbs, which have been lost in their descendents. 

Like horseshoe crabs, tadpole shrimp have a broad semi-circular carapace protecting their heads and are considered living fossils. There are 11 recognised species in two genera, Lepidurus and Triops. The two genera probably diverged about 180 million years ago, but there are fossil tadpole shrimp dating from about 250 million years ago. That's not as long as the really iconic living fossils, like horseshoe crabs and the coelacanths, but it is still an impressive amount of time to retain enough features to be easily recognised as related.

The tadpole shrimp, Lepidurus apus (photo Wikipedia)

The problem with relying on features that preserve in the fossil record is that it underestimates the actual amount of evolutionary change because generally only hard parts are preserved. A recent study of tadpole shrimp highlights this point. Mathers et al. 2013 used genetic analyses to construct the evolutionary relationships among the 11 species of tadpole shrimp. They found that there are actually 38 species and that these species arose relatively recently. This shows that rather than evolutionary stasis, there is likely to be high species turnover in the group.

There are many reasons why some features may be conserved over long periods of time. None of these have to do with natural selection taking a break. In fact, if natural selection did cease we should expect to see features wander under random genetic drift, as has been hypothesised for eyes in cave dwelling animals. Conserved features are much more likely to be the result of developmental constraints or stabilising selection.

References:

Briggs, D., Siveter, D., Siveter, D., Sutton, M., Garwood, R., & Legg, D. (2012). Silurian horseshoe crab illuminates the evolution of arthropod limbs Proceedings of the National Academy of Sciences, 109 (39), 15702-15705 DOI: 10.1073/pnas.1205875109 

Mathers, T., Hammond, R., Jenner, R., Hänfling, B., & Gómez, A. (2013). Multiple global radiations in tadpole shrimps challenge the concept of ‘living fossils’ PeerJ, 1 DOI: 10.7717/peerj.62

Selden, P., Shih, C., & Ren, D. (2011). A golden orb-weaver spider (Araneae: Nephilidae: Nephila) from the Middle Jurassic of China Biology Letters, 7 (5), 775-778 DOI: 10.1098/rsbl.2011.0228