Squid family planning

Female southern bottletail squid may be able to influence the paternity and quality of their offspring by eating the sperm of males. This behaviour is likely to be the result of the conflict that arises between males and females because of their competing evolutionary interests in reproduction. Both sexes use a variety of tactics to manipulate the outcome of mating into their favour. In southern bottletail squid, Sepiadarium austrinum, males use aggression to coerce females into copulations that they might otherwise avoid. 

A new paper from Ben Wegener, Devi Stuart-Fox, Mark Norman and Bob Wong shows that males don’t have it all their own way. Mating occurs head-to-head and is initiated by the male who lunges at the female and grasps her in his tentacles. The male then transfers packets of sperm, called spermatophores, to the female by sticking them into a cavity just below her mouth where they can survive for up to three weeks. But, the spermatophores often have shorter lives because the females will remove and eat them, sometimes before the male has finished copulating with her.

The authors also determined how females were using the nutrients gained from eating the spermatophores. They fed a group of spermatophore-depleted males on a diet laced with a radioactive marker, which was incorporated into new spermatophores as they produced them. Once the females had eaten the radiolabeled spermatophores it was possible to find where the nutrients were being used by assaying for the marker in tissue samples. 

Levels of the marker were elevated in a number of tissues, including the eggs and reproductive glands. Females, therefore, benefit from consuming spermatophores by gaining some additional nutrition that can be allocated to producing offspring. It’s also possible that spermatophore consumption is a form of cryptic female choice, where the spermatophores of low quality males are eaten preferentially. But, this remains to be demonstrated.

This story is also published on the Australasian Evolution Society website in the Research Highlights section.

Reference

Wegener, B. J., Stuart-Fox, D., Norman, M. D., & Wong, B. B. M. (2013). Spermatophore consumption in a cephalopod Biology Letters, 9 (4) DOI: 10.1098/rsbl.2013.0192

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

In the cave of the blind, the no-eyed crab is king

Cave dwelling creatures are often blind. The prevailing view is that, in such species, mutations in the visual system have little or no effect on fitness and vision is lost as these mutations gradually accumulate. There are several other types of characters that we can be reasonably confident are adaptations to life in caves, such as elaboration of structures for touch or smell. However, it is often hard identify which population cave adapted species are descended from and, therefore, how long ago they invaded caves. Without this information it has been hard to test ideas about the evolution of traits associated with life in the dark.

A cave form of the fish, Astyanax mexicanus, which is eyeless and unpigmented, traits typical in caves. It is a commonly used model species in studies of adaptation to cave environments (photo Wikimedia Commons).

Sebastian Klaus and colleagues from the National University of Singapore and Goethe University examined five species of freshwater crab in the genus Sundathelphusa, which occur on Bohol Island in the Philippines. Four species are only found in caves and the other has established several populations in caves. The repeated invasion of caves by the crabs has led to varying degrees of adaptation to life in the dark within the group. 

Freshwater crabs in the genus Sundathelphusa from Bohol Island. Thy are arranged from least cave adapted (top) to most cave adapted (bottom). From top to bottom the species are Sundathelphusa boex, S. vedeniki, S. urichi, S. sottoae and S. cavernicola (from Klaus et al. 2013).

The team used genetic data to estimate the time at which each species and population last shared a common ancestor. They then compared several features of cave-adapted crabs with their closest terrestrial relatives. Reductions in the visual system were just as pronounced as changes in cave-adapted features, indicating that evolution occurs at similar rates. The authors argue that this is a clear sign that eye loss is under directional selection because changes should appear more slowly if they are a result of selectively neutral mutations. 

They don’t speculate at all about what might favour eye-loss in the Bohol crabs, but hint in the introduction that it could be due to trade-offs between vision and other sensory systems. Trade-offs occur where increasing one aspect of fitness necessarily requires the reduction of fitness in another. If eyes are energetically costly to build and maintain then retaining functional eyes might prevent greater investment in other senses. Trade-offs are ubiquitous in biology and have been implicated in the loss of eyes in other cave dwelling species.

While I was doing research on this study I came across several creationist websites that argue cave adapted creatures are strong evidence that evolution is false because a trait is lost. According to them this shows evolution progressing in the wrong direction to what is predicted. They argue that evolution should progress towards more information and greater complexity. This is incorrect and shows, yet again, that creationists typically have a poor understanding of evolutionary theory.

The 'logic' of this argument is similar to the idea of a "Great Chain of Being", which pervaded early thinking about biology. This type of thinking is where we get several antiquated, but persistent terms, such as "missing link" and "highly evolved". It continues to dog evolution in the way that evolutionary information is often presented, such as the placement of organisms more closely related to us at the right or top of phylogenetic trees and at the end of textbooks.

The phylogeny of primates with humans at the top and less related groups at the bottom (from Wikipedia).

Linear descent was never part of Darwin's theory, nor was an increase in information ever a necessary assumption on which evolutionary theory rests. When you look at an evolutionary tree (like the primate tree above), all of the living species at the branch tips have an equally long evolutionary history. They are not descended from each other, they are descended from a common ancestor. You could say that they are equally evolved.

The first evolutionary tree drawn by Darwin over 20 years before the publication of On the Origin of Species.

Evolution doesn't prevent information from increasing, but contrary to the creationist claims it does predict that there will be strong limits on it. Both single trait and multi-trait trade-offs are thought to prevent organisms from becoming perfectly adapted. Single trait trade-offs occur where elaboration of a structure increases fitness in one environment, but reduces it in others. Multi-trait trade-offs occur where two or more structures are dependent on a shared finite resource.

Blind crabs are not evolving in the wrong direction. There is no wrong direction, they're just evolving under the constraint of trade-offs. Eye reduction and loss of pigmentation are not the only evolutionary changes that are occurring either. Other traits are becoming more elaborated, such as the length of their legs and the hairs on their claws, suggesting a multi-trait trade-off. This result is not only consistent with evolutionary theory, but expected.

An abbreviated version of this post is published on the Australasian Evolution Society website in the Research Highlights section.

Reference

Klaus, S., Mendoza, J., Liew, J., Plath, M., Meier, R., & Yeo, D. (2013). Rapid evolution of troglomorphic characters suggests selection rather than neutral mutation as a driver of eye reduction in cave crabs Biology Letters, 9 (2), 20121098-20121098 DOI: 10.1098/rsbl.2012.1098

Research Highlights from the Australasian Evolution Society

I have been asked by the Australasian Evolution Society to provide some 'Research Highlights' for their newly launched website. The Research Highlights promote interesting recent research by evolutionary biologists in Australasia. To get more diversity in the types of research covered there will be two or three others writing too. My stories will go up every few weeks and I will endeavor to publish them here as well, probably with some additional comments. My first piece went up a few weeks ago and I've submitted my second, which should go up shortly. I'll post here as soon as it is.